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I  I  DO  1  D V      f 


MEMOIRS 
OF 

THE  WISTAR  INSTITUTE  OF  ANATOMY   AND   BIOLOGY 

No.  1 


THE  ANATOMY  AND  DEVELOPMENT  OF 

THETSYSTEMIC  LYMPHATIC  VESSELS 

IN  THE  DOMESTIC  CAT 


GEO.  S.jHUNTINGTON 

PROM  THE  ANATOMICAL  Itt^ffEATOBY  OP  COLUMBIA  UNIVERSITY 


PHILADELPHIA,  PA. 
MAY,  1911 


MEMOIRS 
OF 

THE  WISTAR  INSTITUTE  OF  ANATOMY   AND    BIOLOGY 

No.  l 


THE  ANATOMY  AND  DEVELOPMENT  OF 

THE  SYSTEMIC  LYMPHATIC  VESSELS 

IN  THE  DOMESTIC  CAT 


GEO.  S.  HUNTINGTON 

FROM  THE  ANATOMICAL  LABORATORY  OF  COLUMBIA  UNIVERSITY 


PHILADELPHIA,   PA. 
1911 


COMPOSED   AND  PRINTED   AT   THE 

WAVERLY  PRESS 
BY  THE  WILLIAMS  &  WILKINS  COMPANY 

BALTIMORE,  I1.  B.  A. 


CONTENTS 

Introduction     5 

Part  I.     The  development  of  the  systemic  lymphatic  vessels  in  their  relation 

to  the  blood-vascular  system 9 

Historical  review  of  theories  of  lymphatic  development 10 

Material  used  in  present  investigation 16 

Comparison  of  haemal  and  lymphatic  vascular  development 19 

Ontogeny  of  mammalian  systemic  lymphatic  vessels 24 

Mutual  relations  of  developing  systemic  lymphatic  vessels  and  em- 
bryonic veins 27 

Phylogenetic  relations  of  the  abdominal  veins  and  axial  lymphatics  in 

mammals 33 

Development  of  systemic  lymphatic  vessels  in  the  mammal  independ- 
ent of  topographical  association  with  embryonal  veins 49 

Summary  and  conclusions  of  Part  I 53 

Figs.  1  to  28 

Part  II.     The  development  of  the  preazygos  and  azygos  segments  of  the  thor- 
acic ducts 55 

1.  The  thoracic  duct  approach  of  the  jugular  lymph  sacs 60 

Figs  29  to  91. 

2.  The  preazygos  segment 83 

Adult  conditions 84 

Figs.  92  to  99. 

A.  The  development  of  the  broncho-mediastinal  trunk 91 

Figs.  100  to  158. 

B.  The  development  of  the  preazygos  segment  of  the  thoracic  duct 107 

Figs.  159  to  169. 

C.  Junction  of    preazygos   segment   of    thoracic    duct    and  broncho- 

mediastinal  trunk  with  each  other  and  with    the    thoracic    duct 

approach  of  the  jugular  lymph  sac 113 

Figs.  170  to  187. 

3.  Azygos  segment 121 

A.  General  analysis  of  the  development  of  the  thoracic  duct  in  the 

azygos  region 123 

Figs.  188  to  193. 

B.  Detailed  consideration  of  the  individual  stages  in  the  development 

of  the  azygos  segment  of  the  thoracic  duct 129 

Junction  of  azygos  and  preazygos  segments  of  the  thoracic  duct 150 

Figs.  194  to  275. 

Summary  and  conclusions  of  Part  II 153 


INTRODUCTION 

I  have  recently  published  in  a  preliminary  communication,1  a 
re'sume'  of  the  results  obtained  in  an  investigation  of  mammalian 
lymphatic  development  and  organization  extending  over  the 
past  six  years,  and  now,  in  its  main  chapters,  concluded.  The 
paper  above  quoted  was  presented,  with  demonstrations  of 
slides,  at  the  25th  session  of  the  Association  of  American  Anat- 
omists held  in  Boston  during  Convocation  week  of  1910, 
and  is  intended  as  an  attempt  to  definitely  establish  what  I 
believe  to  be  the  genetic  principle  upon  which  all  systemic 
lymphatic  development  in  the  mammalian  embryo  is  based. 
In  outline  this  matter  was  also  presented  and  demonstrated  to 
the  Section  of  Anatomy  and  Embryology  of  the  XVIth  Inter- 
national Medical  Congress  held  at  Budapest,  August-September, 
1909,  and  published  in  the  Proceedings  of  the  Congress.2 

Owing  to  the  character  of  the  problem  and  its  complexity,  a 
detailed  consideration  of  the  same  exceeds  the  reasonable  limits 
of  an  article  suitable  for  publication  in  our  current  anatomical 
periodicals,  and  the  unavoidable  number  of  microphotographic 
illustrations  demanded  makes  publication  through  the  ordinary 
channel  still  more  unadvisable.  For  these  reasons  I  have  ar- 
ranged, with  the  cooperation  of  The  Wistar  Institute  of  Anatomy, 
through  Director  Greenman,  to  publish  the  details  of  my  obser- 
vations on  mammalian  lymphatic  ontogeny  in  the  form  of  a 
series  of  monographs,  in  which  the  subject  can  be  handled  with 

1  G.  S.  Huntington:  "The  Genetic  Principles  of  the  Development  of  the  Sys- 
temic Lymphatic  Vessels  in  the  Mammalian  Embryo."     Anat.   Record.,  vol.  iv, 
no.  11,  1910,  pp.  399  to  403,  with  32  illustrations.     (18  plates.) 

2  G.  S.  Huntington:  "Ueber  die  Entwicklung  desLymphatischen Systems  beim 
Sauger-Embryo."     Compte-Rendu,    xvi.    Congres    International   de   Medecine, 
Section  1,  Anatomic,  Embryologie,  2.  Fascicule,  pp.  127-142,  Budapest,  1910. 


6  INTRODUCTION 

less  restraint  than  in  one  of  the  current  publications.  I  have 
been  led  to  the  undertaking  largely  by  nay  conviction  of  the  value 
of  the  work  which  has  been  done  within  the  last  decade  in  this 
field  by  American  investigators.  The  development  of  the  lym- 
phatic system  is  one  of  the  very  few  broad  morphological 
problems  as  yet  incompletely  solved,  and  I  believe  that  the  pains- 
taking, able  and  conscientious  work  of  the  relatively  large  num- 
ber of  interested  investigators  of  the  subject  in  this  country  will 
eventually  furnish  a  satisfactory  answer  to  the  question,  as  a 
national  contribution  to  the  advancement  of  anatomical  science. 

I  have  been  obliged  to  differ,  on  the  basis  of  my  own  investi- 
gations, from  the  conclusions  reached  by  most  of  my  American 
colleagues.  I  hence  welcome  the  opportunity  of  placing  my  results 
fully  on  record,  in  such  a  manner  that  they  can  be  readily  examined 
and  verified,  if  correct,  or  refuted,  if  found  to  be  erroneous.  In 
carrying  out  this  purpose  it  is  of  course  necessary,  in  order  to 
avoid  repetition  and  economize  space,  to  simply  refer  to  those 
parts  of  the  subject  which  have  been  already  fully  covered  in 
the  existing  publications,  and  to  include  these  articles  as  part 
of  the  entire  record.  The  main  problem  then  is  narrowed  down 
to  the  developmental  history  of  the  mammalian  systemic 
lymphatic  channels,  as  distinguished  from  the  jugular  lymph 
sacs,  or  other  homologous  structures  of  like  origin  and  equivalent 
functional  significance,  wherever  situated. 

The  proposed  series  of  publications  will  include  the  following 
topics  in  the  order  given: 

Part  I.  The  development  of  the  systemic  lymphatic  vessels  in 
their  relation  to  the  blood  vascular  system. 

Part  II.  The  development  of  the  preazygos  and  azygos  segments 
of  the  thoracic  ducts. 

Part  III.  The  development  of  the  visceral  lymphatic  drainage, 
and  especially  of  the  lymphatics  of  the  abdominal  cavity;  the  forma- 
tion of  the  receptaculum,  and  of  the  postazygos  segment  of  the  thor- 
acic ducts,  as  well  as  the  lymphatic  return  from  the  pelvic  and  caudal 
regions  and  from  the  posterior  extremity. 


Part  IV.  The  development  of  the  main  lymphatic  trunks,  other 
than  the  thoracic  ducts,  draining  into  the  jugular  lymph  sacs,  and 
through  them  into  the  venous  system,  viz.,  the  cervical,  jugular  and 
supra-scapular  lymphatics,  and  their  mediastinal  connections,  and 
the  lymphatic  return  from  the  anterior  extremity  along  the  sub- 
clavian  vein. 

Part  V.  The  interpretation  of  adult  normal  and  variant  lym- 
phatic organisation  on  the  genetic  basis,  and  the  interdependence 
of  the  adult  venous  and  lymphatic  systems. 

The  present  publication  includes  Parts  I  and  II  of  the  above 
list. 


PART  I 

THE  DEVELOPMENT  OF  THE  SYSTEMIC  LYMPHATIC 
VESSELS,  IN  THEIR  RELATION  TO  THE  BLOOD- 
VASCULAR  SYSTEM 

The  question  as  to  the  origin  of  the  lymphatic  vessels  has, 
especially  since  1902,  occupied  the  attention  of  a  number  of 
American  observers.  These  investigations  have  followed  the 
older  work  on  the  same  subject  of  Langer  ('68),  Budge  ('80-'87), 
Gulland  ('94),  Ranvier  ('95-'97)  and  Sala  (1900),  and  the  results 
have  been  published  chiefly  in  the  American  Journal  of  Anatomy* 
and  in  the  Anatomical  Record.* 

During  the  progress  of  these  researches  a  number  of  facts  of 
primary  importance  bearing  on  the  problem  of  lymphatic  develop- 
ment and  organization  have  been  discovered.  Some  of  these 
facts  have  been  worked  out  in  detail  and  are  based  on  sufficiently 
extensive  material  and  accurate  observation  to  carry  con- 
viction by  their  constancy  and  consistency  and  to  warrant  their 
acceptance  as  definitely  established  ontogenetic  conditions  in 
the  mammalian  embryo.  Other  observations  still  lack  complete 
confirmation,  and  in  some  others  the  methods  employed  in  their 
determination  create  a  doubt  as  to  their  validity,  and  tend  to 
confuse  the  subject.  Finally  there  are  other  conditions  concern- 
ing which  there  still  exists  an  honest  difference  of  opinion,  and 
which  hence  require  further  study  and  definite  determination. 
On  the  whole,  however,  the  American  work  of  the  last  six  or 
seven  years  has  led  to  considerable  and  permanent  advance  in 

» Vol.  i,  1902;  vol.  iii,  1904;  vol.  iv,  1904;  vol.  v,  1905;  vol.  vi,  1907;  vol.  ix,  1909; 
vol.  x,  1910 
4  Vol.  ii.  1908:  vol,  iv,  1910- 

9 


10         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

our  knowledge  of  the  genesis  of  the  mammalian  lymphatic 
system. 

The  results  so  far  obtained,  and  the  views  based  thereon,  may, 
with  inclusion  of  the  older  work  on  the  subject  of  vertebrate 
lymphatic  development  in  general,  be  briefly  summed  up  as 
follows  in  the  form  of  short  theoretic  statements: 

I.  The  lymphatic  system  is  developed  independently  of  the 
blood-vascular  system.  It  is  formed  by  the  confluence  of  inde- 
pendently developed  mesenchymal  spaces,  and,  in  case  of  the 
avian  thoracic  duct,  by  canalization  of  preformed  solid  strands 
of  differentiated  mesenchyme.6- 6> 7 

The  works  of  Brachet  and  the  combined  researches  of  Brachet 
and  Swaen,8  in  their  relation  to  the  interpretation  of  lymphatic 
development,  also  support  the  independent  origin  of  the  lymph- 
atic system  from  the  mesenchyme. 

The  interesting  observations  of  Marcus  on  the  development  and 
organization  of  the  lymphatic  system  in  Hypogeophis9  place  the 
conclusions  of  this  investigator  in  regard  to  the  genesis  of  lym- 
phatic structures  in  this  general  division,  with  the  addition  of  the 
conception  of  the  coelomata  as  primary  lymphatic  spaces  (vide 
infra,  pp.  25  and  26),  and  the  phylogenetic  derivation  of  the 
peripheral  lymphatic  system  from  the  same. 

8  Budge:  "Ueber  ein  Canalsystem  im  Mesoderm  von  Hiihnerembryonen." 
Arch,  fiir  Anat.  und  Phys.,  Anat.  Abth.,  1880,  s.  320.  "Untersuchungen  iiber 
die  Entwicklung  des  Lymphsystems  beim  Hiihnerembryo."  Arch.  f.  Anat.  u. 
Phys.,  Anat.  Abth.,  1887,  s.  59. 

6  L.  Sala:  "Sullo  sviluppo  del  cuori  linfatici  e  del  dotti  toracici  nell'  embryone 
di  polio,"    Ricerche  fatta  nel  Laboratorio  di  Anatomia  Normale  della  R.  Univ. 
di  Roma,  vol.  vii,  p.  263-269,  April,  1900. 

7  G.  Lovell  Gulland:  "The  Development  of  Lymphatic    Glands",  Jour.    Path, 
and  Boot.,  vol.  ii,  1894,  pp.  447-485. 

8  A.  Brachet,  "Recherches  sur  le  developp.  du  coeur,  des  premiers  vaisseaux 
et  du  sang  chez  les  amphibiens  urodeles,"  Arch,  d'anat.  microscopique,  ii,  1898. 
"Recherches  sur  1'origine  de  1'appareil  vasculaire  sanguin  chez  les  amphibiens," 
Arch,  de  Biologic,  xix,  1903. 

A.  Swaen  et  A.  Brachet,  "Etude  sur  les  premiers  phases  du  developp.  des 
organs  derives  du  mcsoblast  chez  les  poiissons  teleostiens,"  Arch,  de  Biologie, 
xvi,  1899-1900. 

9  H.  Marcus,  "Beitrage  zur  Kenntnis  der  Gymnophionen;  II.  Ueber  interseg- 
mentale  Lymphherzen,  nebst  Bemerkungen  iiber  das  Lymphsystem,"  Morphol. 
Jahrbuch,  Bd.  xxxviii,  Heft  4,  1908. 


RELATION  OF  LYMPHATIC    TO    BLOOD-VASCULAR    SYSTEM         11 

II.  The    lymphatic    vessels    are    directly   derived  from  the 
venous  system,  certain  embryonic  venous  channels  being  trans- 
ferred in  toto  to  the  lymphatic  system.10'11'12-13 

III.  All  systemic  lymphatics  are  formed  by  union  of  multiple 
direct  derivatives  from  the  embryonic  veins,14  or  only  the  thoracic 
ducts  are  so  developed,  while  the  other  systemic  lymphatic  ves- 
sels arise  independently.15 

IV.  The  mammalian  lymphatic  system  as  a  whole  is  developed 
by  blind  ducts  which  "bud  off"  from  the  embryonic  veins  of  the 
cervical,  and  later  from  those  of  the  inguinal  region,  widen  out 
to  form  sacs,  from  which  lymphatics  grow  to  the  skin  and  "cover 
its  surface,  while  at  the  same  time  a  growth  of  ducts  occurs  along 
the  dorsal  line  following  the  aorta  to  make  a  thoracic  duct  from 
which  lymphatics  grow  to  the  various  organs."  The  theory  under- 
lying this  conception  of  lymphatic  development  assumes  the 
primary  formation  of  a  number  of  sacs,  derived  from  the  veins, 
and  lined  by  embryonic  venous  endothelium,  from  which,  as  the 

111  C.  Langer:    "Ueber  das  Lymphgefasssystems  des  Frosches."     Sitzb.  d.  Akad. 
</.  Wissensch,  Bd.  Iviii.,  I.  Abth.,  1868. 

11  L.  Ranvier:    Comptes  Rendues,  1895,  1896.     "Morphologic  et  developpement 
des  vaissaux  lymphatiques  chez  les  mammiferes."      Archives  d' Anatomic  Micro- 
scopique,    Tome  I,  1897. 

12  Giuseppe  Favaro,  "Richerche  intorno  alia  morfologia  ed  allo  sviiuppo  dei 
vasi,  seni  e  cuori  caudali  nei  Ciclostomi  e  nei  Pesci,"  Atti  del  Reali Institute  Veneto 
di  Scienze,  Letters  et  Arti.,    anno  accad.  1905-1906,  Tomo  Ixv,    Parte  seconda. 
Appendice  alia  Dispensa  X.      "Note  fisiologiche  intorno  al  cuore  caudale  dei 
Murenoidi  (Tipo  Anguilla  vulgaris,  Turt.),"    Archiv.  di  Fisiologia,  vol.  ii,  Fasc. 
v,  Luglio,  1905.    "II  cuori  ed  i  seni  caudali  dei  Teleostei,"  Anat..Anz.,  xxvii.  Band, 
no.  14  und  15,  1905. 

13  W.  F.  Allen,  "The  Distribution  of  the  Lymphatics  in  the  Head  and  in  the 
Dorsal,  Pectoral  and  Ventral  Fins  of  Scorpaenichthys  mamoratus,"  Proc.  Wash- 
ington Acad.  of  Sciences,  vol.  viii,  pp.  41-90,  May  18  1906.    "The  Distribution  of 
the  Subcutaneus  Vessels  in  the  Head  region  of  the  Ganoids,  Polyodon  and  Lepi- 
dosteus,"  ibid.,  vol.  ix,  pp.  79-158.  July  1907.     "The  blood-vascular  system  of 
the  Loricati,  the  mail-checked  fishes,"  ibid.,  vol.  vii,  1905. 

"Distribution   of  the  subcutaneous  vessels  in   the  tail   region    of   Lepisos- 
teus,"    Am.  Jour.  Anat.  vol.  viii,  1908. 

14  F.  T.  Lewis:    "The  Development  of  the  Lymphatic  System  in    Rabbits." 
Am.  Journ.  of  Anat.,  vol.  v,  1905,  pp.  95-111. 

15  C.  F.  W.  McClure:  "The  Development  of  the  Thoracic  and  Right  Lymphatic 
Ducts  in  the  Domestic  Cat."     Anat.  Anz.,  xxxii.  Band,  No.  21  and  22,  1908,  p. 
534. 


12         DEVELOPMENT   OF  THE  SYSTEMIC   LYMPHATIC   VESSELS 

starting  points,  the  lymph  channels  of  the  entire  body  develop 
by  a  process  of  continuous  and  uninterrupted  centrifugal  "sp rout- 
ing" toward  the  periphery.16-1 7,  is,  19, 20 

V.  The  systemic  lymphatics  are  formed  by  confluence  of 
perivenous  mesodermal  spaces,  developed,  as  separate  anlages, 
outside  the  intima  of  the  early  venous  channels,  but  not  communi- 
cating with  the  same  except  at  definite  points  of  lymphatico- 
venous  connection  which  are  secondarily  formed.21 

This  view  pronounces  for  the  ontogenesis  of  endothelial  cells, 
lining  the  separate  mesodermal  spaces,  independently  of  the 
haemal  vascular  endothelium.  The  spaces  forming  the  first 
anlages  of  the  systemic  lymphatic  vessels  are  in  no  sense  derived 
from  the  embryonic  veins,  although  closely  associated  with  them 
topographically. 

At  the  time  of  the  publication  of  the  paper  embodying  these 
views,  McClure  and  I  were  not  aware  of  the  important  role 
played  by  the  jugular  lymph  sacs,  as  affording  the  portals  of 
entry  of  the  entire  systemic  lymphatic  circulation  into  the 
venous  system.  This  relation  was  only  subsequently  ascertained 

16  F.  R.  Sabin:  "On  the  Origin  of  the  Lymphatic  System  from  the  Veins,  and 
the  Development  of  the  Lymph  Hearts  and  Thoracic  Duct  in  the  Pig,"  Am.  Jour. 
Anat.,  vol.  i,  1902,  pp.  367-389.     "On  the  Development  of  the  Superficial  Lym- 
phatics in  the  Skin  of  the  Pig,"  Am.  Jour.  Anat.,  vol.  iii,  1904,  pp.  183-195.     "The 
Development  of  the  Lymphatic  Nodes  in  the  Pig  and  the  Relation  to  the  Lymph 
Hearts,"  Am.  Jour.  Anat.,  vol.  iv,  1905,  p.  355-389.      "Further  Evidence  on  the 
Origin  of  the  Lymphatic  Endothelium  from  the  Endothelium  of  the  Blood  Vascu- 
lar System,"     Anat.  Record.,  vol.  ii,  1908,  pp.  46-54.     "The  Lymphatic  System 
in  Human  Embryos,  with  a  Consideration  of  the  Morphology  of  the  System," 
Am.  Jour.  Anat.,  vol.  ix,  1909,  pp.  43-90. 

17  W.  J.  MacCallum:  "Die  Beziehung  der  Lymphgefasse  zum  Bindegewebe." 
Arch.  f.  Anat.  und  Phys.,  Anat.  Abth.,  1902. 

18  G.  Heuer:  "The  Development  of  the  Lymphatics  in  the  Small  Intestine  of  the 
Pig."     Am.  Jour.  Anat.,  vol.    ix,  no.  1,  1909. 

19  W.  A.  Baetjer:  ''The  Origin  of  the  Mesenteric  Lymph  Sac  in  the  Pig."     Anat. 
Record,  vol.  ii,  1908. 

20  H.  Hoyer,  "Untersuchungen  tiber  das  Lymphgefasssystem  der  Froschlarven. 
I.  Theil."     Extrait  du  Bulletin  de  V Academic  des  Sciences  de  Cracovie,  Clissz  des 
Sciences  mathematiques  et  naturelles.     Juillet,  1905.     II.  Theil,  ibid.,  Mai,  1908. 

21  G.  S.  Huntington  and  C.  F.  W.  McClure:  "The  Development  of  the  Main 
Lymph  Channels  of  the  Cat  in  their  Relation  to  the  Venous  System."  Am.  Jour. 
Anat.,  vol.  vi,  1907.     Abstr.  Anat.  Rec.,  vol.  i,  pp.  36-41. 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          13 

in  the  course  of  a  detailed  joint  investigation  of  the  development 
of  these  organs.  We  consequently  failed  to  correctly  recognize 
the  origin  of  the  adult  lymphatico-venous  junctions,  and  regarded 
them  as  direct  secondary  connections  of  the  systemic  lymphatics 
with  the  veins.  The  paper  quoted,  however,  describes  the 
genesis  of  the  lymphatic  vessels  in  their  relation  to  the  venous 
system  correctly. 

VI.  In  1907  I  published,22  based  on  McClure's  and  my  own 
joint  investigations,  a  genetic  interpretation  of  the  development 
of  the  mammalian  lymphatic  system  as  a  whole,  in  which  I  defined 
the  same  as  the  product  of  the  union  of  two  genetically  different 
and  very  unequal  portions: 

1.  The  entire  extensive  system  of  the    lymphatic    vessels 
proper   of   the  adult  animal,  including  the  thoracic  and  right 
lymphatic  ducts  and  their  tributaries,  is  formed  by  the  confluence 
of  extra-venous  intercellular  mesodermal  spaces,  in  the  sense 
above  defined  (V). 

These  spaces  are  lined  by  a  lymphatic  vascular  endothelium 
which  is  not  derived  from  the  haemal  vascular  endothelium,  but 
develops  independently  of  the  same.  The  lymphatic  channels, 
which  result  from  the  confluence  of  these  spaces,  follow  in  large 
part  the  embryonic  veins  closely,  but  they  are  neither  derived 
from  them,  nor  do  they  communicate  with  them,  except  at 
definite  points,  at  which  the  rudimentary  mammalian  type  of 
lymphatico-venous  heart  is  developed. 

2.  A  definite  structure,   the  Jugular  Lymph  Sac,  develops 
in  the  prevalent  and  typical  mammalian  lymphatic  organization, 
directly  from  a  perivenous  capillary  reticulum  of  the  early  pre- 
and  postcardinal  veins,  adjacent  to  and  including  their  point  of 
confluence  to  form  the  duct  of  Cuvier.     This  jugular  lymph  sac, 
or  rudimentary  homologue  of  one  of  the  lymph  hearts  of  lower 
vertebrates,  arising  directly  from  the  veins,  subsequently  separ- 
ates for  a  short  period  entirely  from  the  same,  and  finally  makes 
two  sets  of  permanent  connections: 

22  G.  S.  Huntington:  "The  Genetic  Interpretation  of  the  Development  of  the 
Mammalian  Lymphatic  System."  Anat.  Record,  vol.  ii,  1908,  pp.  19-45. 


14  DEVELOPMENT  OF  THE  SYSTEMIC  LYMPHATIC  VESSELS 

(a)  With  the  above  defined  independently  formed  systemic 
lymphatic  channels  of  the  entire  body. 

(6)  Secondary  connections  with  the  venous  system,  re-entering 
the  same  at  one  or  more  typical  and  constant  points,  and  thus 
forming  the  link  which  finally  unites  the  venous  and  the  lymphatic 
systems,  developed  independently  of  each  other. 

The  above  are,  briefly  summarized,  the  views  of  lymphatic 
development  based  on  recent  observations. 

It  will  be  seen,  as  previously  stated,  that  opinions  still  differ 
as  to  the  origin  of  the  first  lymphatic  anlages  and  their  subse- 
quent method  of  growth,  and  as  to  the  genetic  derivation  of  the 
lymphatic  vascular  endothelium. 

The  following  two  main  questions  are  therefore  still  to  be 
definitely  answered: 

(1)  Is  the  adult  mammalian  lymphatic  system  the  result  of 
continuous  and  uninterrupted  growth  from  one  or  more  central 
points  toward  the  periphery,  or  is  it  genetically  a  channel  system, 
developed  on  the  same  lines  as  the  primary  blood  vascular  sys- 
tem, by  the  confluence  of  a  number  of  originally  separate  and 
independent  anlages? 

(2)  Is  the  lymphatic  vascular  endothelium  of  the  mammal 
derived  from  pre-existing  haemal  vascular  endothelium,  or  is  it 
the  result  of  independent  modification  of  mesodermal    cells? 

It  now  remains  to  answer  definitely  these  questions,  and,  on 
the  evidence  of  sufficiently  extensive  material  and  careful  obser- 
vations, to  clear  the  field  of  theoretical  considerations,  and  to 
establish,  as  far  as  possible,  by  sound  methods  and  on  a  broad 
basis,  the  genesis  of  the  mammalian  lymphatic  system  as  a  whole. 
It  is  evident  that  an  interpretation,  which  assumes  to  fulfill  these 
conditions,  must  be  capable  of  accurately  standing  the  test  of 
both  ontogenetic  and  phylogenetic  consistency. 

Believing,  as  I  do,  and  have,  since  my  first  expression  of  opinion 
on  the  subject,  that  the  principles  embodied  in  the  genetic  inter- 
pretation of  mammalian  lymphatic  development  above  outlined 
(VI)  are  correct,  I  have  undertaken  to  establish  their  truth  by  a 
detailed  critical  study  of  the  lymphatic  system,  both  in  the 
adult  and  in  the  embryo,  in  one  mammalian  form,  the  Domestic 


RELATION  OF  LYMPHATIC  TO   BLOOD-VASCULAR  SYSTEM         15 

Cat,  which  animal,  by  reason  of  its  clear-cut  type  of  venous 
development,23  and  the  great  range  of  its  adult  venous  varia- 
tion,24* 25  seemed  to  me  to  offer  the  best  opportunity  of  viewing 
the  problem  of  mammalian  lymphatic  development  both  from 
the  standpoint  of  its  normal  course  in  a  representative  form,  and 
with  reference  to  the  variant  conditions  imposed  upon  it  by 
correlated  variants  in  the  organization  of  the  main  systemic  veins. 

I  have  been  further  influenced  in  my  selection  of  the  cat 
for  special  and  detailed  study  by  the  fact  that  in  my  experience 
the  embryos  of  this  carnivore  offer  uniformly  histological  pictures 
of  lymphatic  ontogenesis  which  are  far  more  definite,  clean-cut 
and  conclusive  than  those  obtained  in  ungulate,  rodent  or  marsu- 
pial embryos.  I  believe  that  the  cat  is  the  only  known  available 
mammal  in  which  the  facts  of  systemic  lymphatic  development, 
as  set  forth  in  the  following  pages,  could  have  been  definitely 
ascertained.  Guided  by  the  clue  thus  furnished,  it  is  not  diffi- 
cult to  determine,  by  comparison,  the  existence  of  absolutely 
corresponding  developmental  conditions  in  the  embryos  of  the 
pig,  rat,  rabbit,  and  opposum.  But  in  none  of  these  forms  are 
the  typical  genetic  stages  as  clearly  marked  and  the  tissues  as 
definitely  differentiated  as  in  the  cat. 

The  investigation  of  mammalian  lymphatic  development 
divides  itself  naturally,  in  accordance  with  the  postulates  of  the 
genetic  theory  above  advanced  (VI),  into  three  separate  and 
distinct  main  parts: 

(1)  The   development   and   adult    anatomy   of   the  jugular 
lymph  sacs. 

(2)  The  development  and   adult  anatomy    of  the  general 
systemic  lymphatic  vessels. 

23  G.  8.  Huntington  and  C.  F.  W.  McClure :  "The  Development  of  the  Postcava 
and  Tributaries  in  the  Domestic  Cat."     Am.  Jour.  Anat.,  vol.   vi,    1907,   Abstr. 
Anat.  Record,  vol.  i. 

24  VVm.  Darrach:  "Variations  of  the  Postcava  and  its  Tributaries  in  605  Exam- 
ples of  the  Domestic  Cat."     Am.  Jour.   Anat.,  vol.  vi,  no.  3,  1907,  Abstr.  Anat. 
Record,  vol.  i,  p.  30. 

"  G.  S.  Huntington  and  C.  F.  W.  McClure  "The  Interpretation  of  Variations 
of  the  Postcava  and  Tributaries  in  the  Domestic  Cat,  based  on  their  Develop- 
ment." Am.  Jour.  Anat.,  vol.  vi,  1907,  Abstr.  Anat.  Record,  vol.  i,  p.  33. 


16         DEVELOPMENT  OF  THE  SYSTEMIC  LYMPHATIC  VESSELS 

(3)  The  mode  of  union  with  each  other  of  the  two  components 
just  enumerated,  and  the  resulting  establishment  of  a  continuous 
centripetal  lymphatic  vascular  system,  with  definite  and  constant 
terminals  in  the  venous  trunks.  The  first  part  of  this  work  has 
been  completed  in  conjunction  with  Prof.  C.  F.  W.  McClure 
of  Princeton  University.  The  results  of  our  joint  investigation 
on  the  development  and  structure  of  the  jugular  lymph  sacs 
of  the  Cat  have  been  published  in  a  preliminary  account.26  The 
details,  with  critical  analysis  of  a  large  series  of  embryos,  and 
illustrations  of  the  reconstructions  of  all  the  important  stages, 
are  given  in  an  extensive  paper  recently  published.27 

In  these  publications  McClure  and  I  have  definitely  demon- 
strated the  fact  that  in  the  embryo  of  the  cat  the  jugular  lymph 
sacs  develop  as  a  small,  but  vitally  important,  part  of  the  entire 
lymphatic  system,  directly  from  the  pre-  and  postcardinal  veins 
and  their  tributary  plexuses,  near  to  and  including  their  Cu- 
vierian  junction. 

The  genesis  of  the  jugular  lymph  sacs  and  their  share  in  the 
adult  organization  having  been  thus  definitely  established  in 
detail,  I  intend  to  follow  independently  the  second  postulate 
of  the  theory  of  the  composite  character  of  the  adult  mammalian 
lymphatic  system  above  outlined  (VI),  and  to  show  that  the 
jugular  lymph  sacs,  of  direct  venous  origin,  constitute  the  links 
uniting  the  haemal  vascular  system  and  the  general  system  of 
the  lymphatic  vessels,  the  latter  developed  independently  of  the 
veins,  by  the  confluence  of  intercellular  mesenchymal  spaces 
surrounding,  for  the  most  part,  the  embryonic  venous  channels, 
but  in  no  sense  derived  from  the  same. 

MATERIAL 

For  the  reasons  stated  above  I  have  chiefly  used  the  embryos 
of  the  domestic  cat.  Of  these  I  have  examined  the  following 
107  individual  embryos  in  complete  serial  sections: 

26  G.  S.  Huntington  and  C.  F.  W.  McClure:  "The  Anatomy  and  Development 
of  the  Jugular  Lymph  Sacs  in  the  Domestic  Cat."    Anat.  Record,  vol.  ii,  1908, 
pp.  1-18. 

27  American  Jour,  of  Anat.,  vol.  x,  no.  2,  April,  1910,  pp.  177  to  311  with  67  figures. 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM 


17 


SERIES  NO. 


CROWN    RUMP 


86  

13  Somites 

CROWN  RUMP 

MEASURE 

(TAKEN 

AFTER 

FIXATION) 

mm. 

82  

4.5 

93  

4.5 

226...  

5.18 

110  

5.6 

138  

5.6 

103  

5.7 

84  

6 

85  

6 

115  

6 

116  

6 

117..  

6 

128  

6 

187  

6 

109  

6.2 

129  

6.5 

130  

6.5 

131  

6.5 

186  

6.5 

105  

6.8 

135  

7 

137  

7 

108  

7.2 

119  

7.2 

121  

7.2 

89  

8 

102  

8 

75A  

8.5 

106  

9 

136  

9.2 

132  

9.5 

133  

9.5 

239  

9.5 

79  

10 

101  

10 

Ill  

10 

112  

10 

113  

10 

114  

10 

140  

10 

237  

10 

81.. 

10.3 

MEASURE 

(TAKEN 

AFTER 

FIXATION) 

SERIES  NO. 

mm. 

118  

10.5 

120  

10.5 

77  

11 

98  

11 

213  

11 

256  

11.5 

78  

12 

97  

12 

100  

12 

217  

12 

92  

13 

107  

13 

76  

13.5 

189  

13.5 

223  

13.5 

127  

14 

210  

14 

211  

14 

212  

14 

214  

14 

75  

.  15 

91  

15 

216  

15 

218  

15 

219  

15 

243  

15 

244  

15 

245  

15 

246  

15 

141  

15.5 

143  

15.5 

215  

15.5 

247  

15.5 

95  

16 

96  

16 

222  

16 

224  

16 

230  

16 

248  

16 

240  

16.5 

94  

17 

142  

17 

198  

17 

258  

.  17 

18          DEVELOPMENT  OF  THE   SYSTEMIC  LYMPHATIC  VESSELS 


CROWN  RUMP  CHOWN  RUMP 


SERIES  NO. 

87            .  -    .  . 

MEASURE 

(TAKEN 

AFTER 

FIXATION) 
mm. 

18 

88       

18 

199         

18.5 

249 

18.5 

250          

18.5 

254      

18.5 

80              .     . 

19 

197 

19 

252            ..     . 

19 

253.  .  . 

.   19 

SERIES  NO. 

83            .  .     .  . 

MEASURE 

(TAKEN 

AFTER 

FIXATION) 
mm. 

20 

255  

20 

241           

20 

242  

21 

147  

2.r> 

168 

34 

144            .  .     .  . 

31.5 

90 

.  .  35 

104... 

.  51 

These  embryos  are  contained  in  the  Embryological  Collection 
of  Columbia  University.  The  majority  of  the  preparations  were 
fixed  in  Zenker's  fluid  and  stained  differentially  on  the  slide 
with  Hsemotoxylon  (Delafield)  and  Orange-G. 

I  have  also  had,  through  the  courtesy  of  Professor  McClure, 
the  opportunity  of  carefully  examining  three  very  interesting 
cat  embryos  of  the  Princeton  Collection,  series  34  and  37,  each 
of  14  mm.  crown-rump  measure,  and  series  53,  a  15mm.  embryo. 

A  series  of  180  adult  animals  with  successful  injection  of  the 
main  systemic  lymphatics  served  as  control  for  the  embryologi- 
cal  determinations,  and  for  the  comparison  of  normal  and  variant 
adult  conditions  of  the  venous  and  lymphatic  systems  with  the 
corresponding  ontogenetic  stages. 

The  results  of  my  observations  on  the  development  of  the 
mammalian  systemic  lymphatic  vessels,  as  distinguished  from 
the  jugular  lymph  sacs,  studied  jointly  with  McClure,  may  be 
briefly  summed  up  as  follows: 

The  systemic  lymphatic  vessels  of  the  entire  body  are  formed 
through  confluence  of  numerous  originally  separate  intercellular 
mesodermal  spaces,  which  develop  iij  great  part  in  close  apposi- 
tion to  the  walls  of  the  embryonic  venous  channels,  and  in  exactly 
the  same  way  as  the  primary  anlages  of  the  haemal  vascular 
system,  but  independent  of  the  latter.  The  endothelium  lining 
these  first  anlages  of  the  lymphatic  vascular  channels  is  from  the 


RELATION  OF  LYMPHATIC  TO   BLOOD-VASCULAR  SYSTEM          19 

beginning  independent  of  the  haemal  endothelium,  and  develops 
with  the  first  appearance  of  the  lymphatic  spaces,  from  the 
indifferent  mesodermal  cells  lining  these  spaces.  In  my  opinion 
the  lymphatic  and  haemal  vascular  endothelium  have  the  same  ge- 
netic derivation  from  the  modified  mesodermal  cell  lining  the  tissue 
spaces.  The  primary  stage  of  endothelial  differentiation  is  the 
same,  whether  the  resulting  channel  system  is  to  be  assigned  to 
the  haemal  or  the  lymphatic  division  of  the  vascular  system. 
We  have  therefore  two  generations  of  the  embryonic  vascular 
endothelial  cell,  a  haemal  and  a  lymphatic.  Both  develop  in 
the  same  way  and  as  the  result  of  identical  genetic  factors  from 
the  indifferent  mesodermal  cell.  Both  are  from  the  very  begin- 
ning of  the  process  independent  of  each  other  in  the  mammalian 
embryo. 

I  desire  again  to  emphatically  aver  my  conviction  that  all  the 
systemic  lymphatic  vessels  of  the  mammalian  embryo,  includ- 
ing the  thoracic  ducts  and  their  tributaries,  are  neither  in  their 
genesis  continuous  " outgrowths"  or  "buds"  from  sacs  of  venous 
origin,  wherever  situated,  nor  derived  from  multiple  outgrowths 
from  the  embryonic  veins,  such  outgrowths  subsequently  separat- 
ing from'the  veins  and  fusing  into  continuous  lymphatic  channels. 
They  are,  in  my  opinion,  on  the  contrary,  from  their  very  first 
inception,  independent  of  the  haemal  vascular  system,  and  their 
endothelial  lining  is  not  derived  from  the  blood  vascular  endo- 
thelium. They  develop  as  independent  intercellular  mesodermal 
spaces,  which  become  confluent  with  each  other  to  form  larger 
and  larger  communicating  channels.  These  finally  attain  their 
entrance  into  the  venous  system  through  the  intervention  of 
the  jugular  lymph  sacs,  in  the  manner  outlined  in  the  publica- 
tions above  quoted. 22>26>27 

Before  taking  up  the  details  of  the  development  of  the  first 
lymphatic  anlages  in  the  mammalian  embryo,  it  seems  advisable 
to  refer  briefly  to  a  resume  of  known  facts  in  regard  to  the  earliest 
formative  stages  of  the  blood  vascular  system,  in  order  to  facili- 
tate the  comparison  between  haemal  and  lymphatic  development. 

Phylogenetically,  the  earliest  form  of  a  closed  circulatory 
system  in  multicellular  organisms  consists  of  intercellular  canals 


20          DEVELOPMENT  OF  THE  SYSTEMIC   LYMPHATIC  VESSELS 

conveying  a  clear  plasmatic  fluid  without  cellular  contents. 
The  same  picture  is  presented  in  the  earliest  stages  of  haemal 
development  in  vertebrates.  Thoma's28  investigations  of  the 
histogenesis  of  the  blood  vascular  system  in  chick  embryos  have 
furnished  us  with  a  very  clear  picture  of  the  process. 

The  first  histogenetic  inception  of  the  vertebrate  haemal 
vascular  system  is  marked  by  the  condensation  of  the  mesoderm 
into  cellular  strands.  Between  the  cells  of  these  praevascular 
strands  multiple  oval  or  round  spaces  develop,  which  enlarge, 
elongate  and  become  confluent,  forming  a  network  of  inter-com- 
municating channels,  the  hcemal  capillary  anlages.  These  chan- 
nels contain  a  clear  colourless  fluid,  with  no,  or  only  very  scat- 
tered, cellular  elements.  This  fluid,  obtained  by  secretion  from 
the  free  surfaces  of  the  cells  limiting  the  spaces,  is  evidently 
under  a  certain  definite  pressure,  which  exerts  an  influence  on 
the  form  of  the  cells  lining  the  channels.  These  limiting  cells 
lose  their  earlier  isodiametric,  more  or  less  regular  cuboidal  form, 
and  appear  flattened,  and  on  optical  section  spindle-shaped. 
They  have  begun  to  assume  the  endothelial  character.  Hence 
from  its  earliest  inception  the  endothelial  lining  of  vascular 
channels  appears  as  an  environmental  adaptation  of  the  meso- 
dermal  cell.  One  surface  of  a  cuboidal  cell  is  freed  from  con- 
tact with  adjacent  cells  by  the  development  of  an  intercellular 
cleft,  and  this  free  surface  is  subjected  to  the  pressure  of  the 
fluid  contained  in  the  earliest  capillary  anlages,  modified  by  the 
tension  pressure  of  the  organism  as  a  whole.  This  mechanical 
adaptation  to  the  altered  cellular  milieu  results  in  the  formation 
of  endothelium,  and  the  process  is  identical  in  all  portions  of 
the  mesoderm,  independent  of  the  question  as  to  whether  the 
resulting  endothelial  lined  space  shall  subsequently  be  incor- 
porated in  a  haemal  or  a  lymphatic  system  of  vascular  channels, 
or  shall  remain  as  a  closed  non-vascular  mesodermal  space. 

It  seems  to  me  futile  to  try  to  speculate  on  an  ontogenetic 
stage  in  which  endothelium  acquires  a  " specific"  character.  It 

28  R.  Thoma:  "Untersuchungen  iiber  die  Histogenese  und  Histomechanik  des 
Blutgefasssystems."  Stuttgart,  1893. 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM         21 

develops  de  novo  in  the  adult  under  appropriate  normal  con- 
ditions. 

Furthermore,  this  endothelial  characterization  of  modified 
mesodermal  cells  is  from  the  beginning  a  multiple  process,  start- 
ing independently  at  innumerable  separate  and  discrete  points 
of  the  vascular  area,  and  becoming  only  subsequently  continuous 
by  confluence  of  the  individual  separate  anlages.  This  fact  is 
of  importance  in  drawing  general  conclusions  as  to  the  later 
extension  of  vascular  endothelium,  whether  haemal  or  lymphatic. 

Up  to  this  point  the  histogenetic  and  physical  characters  of 
all  developing  vascular  structures  are  identical.  The  picture 
just  described  applies  equally  to  the  earliest  definite  anlages  of 
the  haemal  capillary  system,  and,  as  I  shall  show,  to  the  first 
appearance  of  the  earliest  lymphatic  structures  of  the  body. 
In  the  case  of  the  definite  blood-vascular  channels  of  the  verte- 
brate embryo,  however,  a  further  developmental  change  occurs, 
namely,  the  addition  of  free,  specially  modified,  mesodermal 
cells,  as  the  red  blood  cells,  to  the  clear  plasma  circulating  in  the 
channel-system  of  the  earliest  capillary  anlages  in  response  to 
the  first  pulsations  of  the  heart. 

The  first  blood  vessels  of  the  area  pellucida  appear,  at  least 
in  part,  to  develop  independentlyof  the  so-called  "  Blood  islands." 
These  latter,  originally,  form  broad  cellular  strands  composed  of 
closely  packed  uncolored  cells,  which  are  only  distinguished  from 
the  solid  strands  of  the  earliest  vascular  anlages  of  the  area  pellu- 
cida by  greater  size  and  massiveness.  After  the  vascular  cell- 
strands  of  the  area  pellucida  have  developed  in  their  interior  the 
intercellular  closed  oval  or  round  spaces  of  the  first  capillary  an!  ages, 
similar  spaces  also  appear  in  the  more  massive  cell  strands  of  the 
peripheral  portion  of  the  area  vasculosa.  In  the  subsequent 
confluence  of  these  discretely  developed  spaces  to  form  the  early 
capillary  reticulum,  the  blood  islands  become  more  and  more 
surrounded  by  the  forming  channels  and  are  thus  separated  from 
the  adjacent  tissues.  New  endothelial-lined  spaces  continue  to 
develop  on  the  surface  of  the  blood-islands,  enlarge  and  join  the 
system  of  connected  channels.  The  cells  forming  the  walls  of 
these  primitive  capillaries  become,  as  above  stated,  transformed 


22  DEVELOPMENT  OF  THE   SYSTEMIC  LYMPHATIC  VESSELS 

into  the  typical  flattened  endothelial  cells  of  the  vascular  intima. 
Excepted  from  this  endothelial  transformation  are  only  those 
cells  of  the  vascular  walls  which  differentiate  as  young  blood  cells. 
Thus  eventually  the  confluence  of  the  originally  individual  and 
separate  spaces  produces  a  continuous  and  connected  channel 
system,  lined  by  endothelium,  which  nearly  encircles  the  blood 
islands.  The  latter  are  therefore  now  in  large  part  included  within 
the  lumen  of  the  capillaries,  with  whose  walls  they  are  from  place 
to  place  continuous.  It  only  requires  a  further  and  complete 
solution  of  this  continuity,  and  the  accompanying  freeing  of  the 
blood  cells,  to  add  the  latter  to  the  plasma  circulating  in  the 
preformed  channels.  In  the  chick,  according  to  Thoma's  obser- 
vations, the  resolution  of  the  blood  islands  into  separate  blood 
cells  occurs  between  the  45th  and  55th  hour  of  incubation,  while 
the  acquisition  of  haemoglobin  by  the  cells  occurs  between  the 
40th  and  45th  hour.  With  this  occurrence  the  development  of 
the  primary  blood-vascular  channels  has  reached  its  definite 
accomplishment. 

The  general  picture  presented  by  the  earliest  development  of 
the  blood-vascular  system  may  therefore  be  summarized  as  follows: 

(1)  Differentiation  of  certain  mesodermal  areas  and  lines  by 
the  multiplication  of  mesodermal  cells  to  form  cell-strands  of 
varying  density  and  size  (vascular  strands). 

This  appears  to  be  a  common  antecedent  condition  not  only 
of  all  vascular  mesodermal  structures,  but  also  of  other  meso- 
dermal derivatives  eventually  destined  to  obtain  a  lumen  and 
enter  into  the  formation  of  canals,  as  the  Wolffian  tubules  and 
the  cell-strands  of  the  gonad. 

It  possibly  explains  the  conditions  described,  for  example,  by 
Sala  in  the  development  of  the  avian  thoracic  duct,  is  seen 
in  the  developing  aortae  of  early  chick  embryos,  and  is  especially 
significant  in  the  pictures  furnished  by  Sabotta  of  the  develop- 
ment of  the  aortse  in  fishes. 

(2)  Development  in  the  interior  of  these  cellular  strands  of 
intercellular  spaces  in  large  numbers. 

(3)  Bio-mechanical  modification  of  cells  lining  these  spaces 
to  produce  typical  flattened  vascular  endothelium. 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM         23 

(4)  Confluence    of    these    endothelial-lined  spaces  to   form 
larger  and  larger  vascular  areas  of  intercommunicating  channels, 
containing  a  clear  plasmatic  fluid,  which  circulates  in  the  chan- 
nels in  response  to  the  establishment  of  cardiac  pulsation. 

(5)  Addition  to  the  plasmatic  contents  of  these  channels, 
coincident  with  their  further  growth  and  extension  into  a  con- 
tinuous circulatory  system,  of  cellular  elements,  derived  from 
the  mesoderm  and  specially  modified  to  acquire    haemoglobin 
and  function  as  red  blood  cells.     These  cells,  by  solution  of 
tissue  continuity,  are  liberated  from  the  blood  islands  which  are 
first  surrounded  by  the  confluent  spaces  of  the  capillary  anlages. 

(6)  Subsequent  differentiation  of  the  adventitia,  with  speciali- 
zation of  districts  by  cardiac  concentration,  amalgamation  of 
the  plexus  into  larger  arterial  and  venous  channels,  definition 
of  permanent  capillary  areas,  valve  and  septal  formation,  etc. 

The  striking  features  of  this  ontogenetic  history  of  the  blood 
vascular  system  are: 

1.  The  relatively  late  addition  to  the  preformed  non-cellular 
circulation  of  free  cell  elements,  which,  as  the  red  blood  cells, 
stamp,  from  the  period  of  their  liberation  and  inclusion  in  the 
circulating  plasma,  the  resulting  vascular  system  as  haemal. 

2.  The  common  origin  from  mesoderm  of  both  characteristic 
components  of  the  haemal  system,  viz.,  the  vascular  endothelium 
and  the  red  blood  cell.     Both  the  vascular  intima  and  the  free 
cell  contents  of  the  channels  lined  by  this  intima  appear  as  highly 
modified  derivatives  of  the  same  mesodermal  cellular  ancestors, 
which  constitute  the  cell-strands  of  the  earliest  period  of  vascular 
development.         In  their  first  inception  the  systemic  lymphatic 
vessels  of  the  mammalian  embryo,  as  distinguished  from  the 
jugular  lymph  sacs  of  venous  origin,  repeat  in  every  detail  the 
primary  stages  of  the  developing  haemal  capillaries,  prior  to  the 
inclusion  within  the  lumen  of  the  latter,  of  the  cellular  contents 
of  the  blood  islands.     They  can  be  identified  as  distinct  struc- 
tures as  soon  as  the  blood  channels  proper  have  differentiated. 
Before  that  period  direct  observation  cannot  determine,  in  case 
of  individual  mesenchymal  spaces,  whether  they  are  eventually 
to  become  part  of  the  lymphatic  or  of  the  blood  vascular  system. 


24        DEVELOPMENT  OF  THE*  SYSTEMIC   LYMPHATIC   VESSELS 

It  is  therefore  quite  possible  that  in  the  mammalian  embryo  both 
sets  of  intercellular  mesodermal  spaces  develop  side  by  side  and 
simultaneously,  although  prior  to  the  setting  free  of  the  haemo- 
globin cells  and  their  appearance  within  the  lumen  of  the  haemal 
capillaries,  there  is  no  absolute  criterion  which  would  serve  to 
distinguish  intercellular  spaces  as  belonging  definitely  to  either 
the  haemal  or  the  lymphatic  division  of  the  general  vascular 
anlage. 

It  hence  appears  to  me  futile  to  base  serious  conclusions  in 
regard  to  the  genesis  of  vascular  structure  on  observations  laade 
on  the  vessels  seen  in  the  transparent  tails  of  living  anure  am- 
phibia. Phylogenetically,  from  the  urodele  standpoint,  such 
larvae  are  adult  organisms.  We  all  know  that,  once  established, 
all  divisions  of  the  vascular  organization  are,  under  the  stimulus 
of  normal  or  abnormal  growth,  capable  of  further  increase  and 
extension.  The  observations  above  referred  to  may  offer,  if 
correctly  interpreted,  interesting  side  lights  on  the  method  of 
vascular  growth,  but  they  cannot,  in  any  valid  sense,  bear  on 
the  problem  of  vascular  genesis,  either  haemal  or  lymphatic. 

But  in  mammalian  embryos  of  the  proper  stages,  and  specifi- 
cally in  embryos  of  the  Cat  between  10  and  12  mm.,  the  first 
systemic  lymphatic  anlages  are  clearly  differentiated  in  the  cir- 
cumscribed areas  of  their  first  appearance,  coincident  with  the 
definition  of  the  early  intra-embryonic  blood  channels. 

Thus  in  the  omphalo-mesenteric  district,  and  cephalad  and 
caudad  of  this  point,  on  each  side  of  the  aorta,  isolated 
intercellular  mesenchymal  spaces  appear  at  this  period,  closely 
applied  to  the  walls  of  the  neighboring  venous  plexuses  of  the 
postcardinal  and  mesonephroic  veins,  but  not  connected  with 
the  same.  These  intercellular  clefts  enlarge  rapidly  to  form 
numerous  oval  or  round  spaces,  closely  interwoven  with  the 
venous  network  and  later  with  the  sympathetic  anlages.  The 
cells  limiting  these  early  lymphatic  anlages  become,  with  the 
further  extension  of  the  spaces  which  they  line,  flattened  and 
assume  typical  endothelial  characters. 

Fig.  1  shows  a  transverse  section  of  a  10  mm.  cat  embryo 
(series  111,  slide  viii,  section  4)  magnified  175  diameters,  cephalad 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          25 

of  the  mesonephros  and  the  subcardinal  cross  anastomosis,  and 
gives  a  topographical  view  of  the  region  in  which  the  first  meso- 
dermal  intercellular  lymphatic  tissue  spaces  (77)  appear,  in  the  in- 
terval between  aorta  (73),  postcardinal  vein  (68}  and  coelom  (78}. 

Fig.  2  is  the  same  section  of  this  embryo,  magnified  300  dia- 
meters, and  shows  the  area  to  the  left  of  the  aorta.  Between 
this  vessel  (73}  and  the  well  defined  left  postcardinal  vein  (68} 
dorsad,  and  the  ccelom  cavity  (78}  ventrad,  appear  a  number 
of  clear  mesenchymal  spaces  (77)  which  do  not  communicate  with 
the  adjacent  venous  channels.  Some  of  these  spaces  extend 
from  the  ccelom  angle  dorsad  along  the  lateral  aspect  of  the 
postcardinal.  They  are  the  first  distinctly  recognizable  anlages 
of  the  lymphatic  system,  and  they  develop,  from  their  first 
inception,  as  independent  mesenchymal  spaces,  closely  related 
to  the  adjacent  haemal  channels,  but  genetically  independent 
of  the  latter. 

Fig.  3  shows  the  same  field  in  a  magnification  of  600  diameters. 
The  spaces  are  clearly  cut,  separate  and  distinct,  and  the  limit- 
ing cells  are  beginning  to  assume  endothelial  character. 

The  relation  between  the  haemal  channels  and  the  develop- 
ing adjacent  lymphatic  spaces  can  be  clearly  traced  in  succes- 
sive sections  of  this  same  embryo  proceeding  caudad. 

Figs.  4,  5,  6,  and  7  show,  respectively,  sections  7,  8,  9  and  10 
of  slide  viii  of  series  111,  magnified  300  diameters. 

In  all  of  these  sections  the  uniformity,  and  the  distinct  struc- 
tural character  of  the  primary  lymphatic  tissue-spaces  is  clearly 
visible  in  the  same  situation  and  in  identical  relation  to  surround- 
ing structures. 

For  comparison  with  the  preceding  series  the  same  region  is 
shown  in  another  10  mm.  embryo  (series  120,  slide  ix,  sections 
25  and  26)  in  two  successive  sections,  magnified  300  diameters, 
in  figs.  8  and  9. 

In  these  sections  the  same  independent  mesodermal  spaces 
(77)  are  seen  in  their  typical  relation  to  aorta  (73),  post-cardi- 
nal vein  (68}  and  ccelom  cleft  (75). 

The  interesting  question  of  the  relationship  between  these 
early  mesenchymal  spaces  and  the  coalom  cavity  can  only  be 


26         DEVELOPMENT    OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

considered  superficially  at  this  time.  Yet,  in  some  regions, 
very  suggestive  pictures  are  obtained.  Thus  in  section  4  of 
slide  viii  of  series  111  (figs.  1,  2  and  3)  the  distinct  appearance 
of  a  communication  between  the  coelom  cavity  proper  (78}  and 
the  early  mesenchymal  spaces  (77)  above  described  is  given  by  a 
clearly  limited  and  well  defined  funnel-shaped  stoma,  occuping 
the  dorsal  extremity  of  the  coelomic  cleft  (79  in  fig.  2),  and 
apparently  opening  directly  into  the  spaces  of  the  early  lym- 
phatic plexus.  The  remaining  sections  of  this  series  figured 
(figs.  4  to  7)  confirm  this  impression. 

The  conditions  here  described  for  early  embryos  of  the  cat 
strongly  support  the  views  expressed  by  Marcus9  in  his  studies 
on  the  lymphatic  development  of  Hypogeophis.  The  micropho- 
tographs  here  given  should  be  compared  with  his  description  on 
pp.  599-601  of  the  paper  quoted,  with  his  text  fig.  6,  and  with  his 
figs.  5  and  6  of  plate  xvi. 

The  early  mesodermal  spaces  here  described  and  figured  are 
lymphatic  in  character  and  form  part  of  the  extensive  temporary 
network  of  lymphatic  channels  which  appears  for  a  time  during 
mammalian  ontogenesis  and  which  bears  a  close  resemblance  to 
the  corresponding  lymphatic  organization  in  amphibia  and 
reptiles.  The  peri-aortic  lymphatic  sinuses  and  the  exaggerated 
subcutaneous  lymph  channels  of  the  earlier  mammalian  stages  are 
portions  of  this  evanescent  and  reminiscent  system,  which  subse- 
quently in  large  part  retrogrades,  and  either  disappears  altogether 
or  is  extremely  modified  to  meet  the  definite  permanent  condi- 
tions of  mammalian  lymphatic  organization.  Thus  the  early 
periaortic  spaces  become  much  reduced  in  course  of  further  devel- 
opment. They  then  become  associated,  in  a  way  presently  to 
be  described  in  detail,  with  elements  of  the  axial  venous  plexuses 
of  the  mammalian  embryo  and  form  the  anlages  of  the  main 
segments  of  the  thoracic  ducts.  This  ontogenetic  temporary 
recall  of  antecedent  phylogenetic  types  of  vascular  development 
appears  to  be  chiefly  centered,  in  the  mammalian  embryo,  in 
the  region  around  the  omphalo-mesenteric  artery,  where,  in  the 
adult,  the  definite  and  permanent  lymphatic  trunks  closely 
resemble  in  their  arrangement  the  peri-omphalo-mesenteric 
annular  veins  of  certain  reptilian  embryos. 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          27 

In  the  succeeding  stages  the  mesodermal  lymphatic  anlages 
assume,  in  large  part,  the  Very  definite  relation  to  certain  embry- 
onic venous  channels,  which  led  McClure  and  myself  to  describe 
them  in  1906  in  our  preliminary  account  above  quoted,21  as 
"extraintimal"  or/'perivenous"  structures. 

This  relationship  is  of  two  kinds: 

A.  Total  replacement  of  temporary  embryonic  veins  by  extrainti- 
mal  lymphatic  channels. 

In  t"he  earlier  embryonic  stages  the  areas  of  the  future  definite 
venous  channels  are  largely  occupied  by  an  antecedent  venous 
or  capillary  network,  out  of  which,  along  definite  hydrostatic 
lines,  the  subsequent  veins  develop  by  confluence  of  the  plexus  ele- 
ments occupying  these  lines.29  Parts  of  the  early  capillary  reticu- 
lum,  not  thus  included  in  the  path  of  the  definitely  organized 
venous  trunks,  remain,  after  the  latter  have  become  established, 
as  a  perivenous  plexus.  Some  of  the  elements  of  this  secondarily 
established  plexus  develop  into  permanent  tributaries  of  the 
main  veins.  Others  undergo  a  process  of  separation  from  the 
permanent  functional  channels  and  degenerate.  In  many  cases 
their  blood-cell  contents  break  down  and  are  eliminated,  while 
their  endothelial  lining  appears  to  revert  to  the  indifferent  type 
of  the  embryonic  mesodermal  cell. 

Thus  in  embryos  between  13.5  and  16  mm.  many  striking 
instances  of  this  reversion  are  to  be  observed.  Thp  former 
vascular  channel  appears  as  a  collection  of  clearly  differentiated 
and  very  highly  stained  mesodermal  cells. 

Figs.  47,  50,  51,  in  Part  II,  show  these  mesodermal  vascular 
derivatives  very  clearly.  They  form  the  dark  masses  seen  in 
the  field  dorsal  and  dorsolateral  to  the  O3sophagus  and  in  the 
peritracheal  region. 

In  many  regions  of  the  mammalian  embryo,  however,  these 
detached  and  retrograding  venous  elements  do  not  attain  this 
condition,  but  in  an  earlier  stage,  constitute  lines  around  which  the 
most  active  primary  lymphatic  organization  of  the  mammalian 

a*  H.  v.  W.  Schulte  and  Fred.  Tilney :  "Note  on  the  Organization  of  the  Venous 
Return,  with  Especial  Reference  to  the  Iliac  Veins."  Anal.  Record,  vol.  iii,  no. 
11,  1909. 


28  DEVELOPMENT  OF  THE  SYSTEMIC  LYMPHATIC  VESSELS 

embryo  centers.  The  intercellular  mesodermal  clefts  above 
described  develop  especially  along  and  around  these  decadent 
venules  and  finally  envelop  them.  As  the  result  of  this  process  the 
lymphatic  anlages  appear  in  certain  mammalian  ontogenetic 
stages,  in  large  part,  as  distinct  spaces  enclosing  the  remnant  of 
the  embryonic  vein.  The  latter  may  still,  for  a  time,  contain  a 
few  degenerating  red  blood  cells,  but  these  soon  disappear,  and 
then  the  entire  anlage  is  formed  by  a  collapsed  and  empty  en- 
dothelial  tube,  the  abandoned  channel  of  the  earlier  vein,  sur- 
rounded by  a  second  endothelial  tube,  formed  by  the  confluence 
of  the  independently  developed  extraintimal  or  peri  venous  meso- 
dermal spaces.  As  these  spaces  enlarge  and  join  each  other  their 
lumen  increases,  and  the  limiting  cells  become  flattened  and 
assume  typical  endothelial  characters.  The  height  of  this  phase 
of  lymphatic  development  is  reached  in  embryos  of  the  cat  in  the 
14  mm.  stage,  and  numerous  demonstrations  of  the  appearance  of 
the  structures  on  section  are  given  in  Part  II  of  this  paper.  The 
remnant  of  the  embryonic  vein  bears  a  relation  to  the  replacing 
perivenous  lymphatic  channel  which  is  exactly  the  same  as  that 
of  a  collapsed  inner  tube  to  the  enveloping  shoe  of  a  pneumatic 
tire.  The  inner  skin  of  the  shoe  and  the  rim  of  the  wheel  repre- 
sent the  lymphatic  intimal  endothelium.  The  space  between  the 
shoe  and  the  collapsed  inner  tube  is  the  lumen  of  the  future 
lymphatic  channel.  The  empty  inner  tube  itself  is  the  decadent 
embryonic  vein  upon  and  around  which  the  secondary  lymphatic 
channel  is  built.  In  the  course  of  further  development  the  venous 
remnant  disintegrates  and  disappears,  leaving  a  clear  lumen  for 
the  lymphatic  vessel,  which  thus  completely  replaces  the  earlier 
vein  and  comes  to  occupy  absolutely  the  topographical  position 
of  the  latter. 

Often  the  replacing  lymphatic  begins  as  an  extraintimal 
channel  partially  surrounding  the  receding  vein.  This  leads 
in  course  of  further  development  to  an  expansion  of  the  lymphatic 
channel  not  concentric  with  the  axial  line  of  the  shrinking  vein. 
The  remnant  of  the  vein  then  retires  to  a  point  on  the  intimal 
surface  of  the  new  lymphatic  channel,  and  appears  to  project 
into  the  lumen  of  the  latter.  The  resulting  histological  picture 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM 


29 


will  depend  on  the  plane  of  section  in  reference  to  the  course  of 
the  lymphatic  and  its  contained  venous  remnant.  Thus,  as 
shown  in  the  following  schema,  many  sections  give  the  appear- 
ance indicated  in  1.  If  the  plane  of  section  should,  however,  lie 
in  the  line  A  B,  it  will  divide  the  shrinking  vein  (4)  and  the  envel- 
oping lymphatic  (5)  in  such  a  way  as  to  produce  the  picture  shown 
under  2.  In  other  cases  the  lymphatic  spaces  unite  around 
the  entire  circumference  of  the  abandoned  venule,  and  the  lumen 
is  then  contained  for  long  distances  entirely  within  the  lumen 
of  the  replacing  lymphatic  channel. 


The  process  just  described  is  remarkably  constant  and  uniform 
in  the  critical  stages  of  mammalian  lymphatic  development. 
As  can  be  readily  seen  in  following  the  individual  sections  in 
the  microphotographs  published  in  Part  II,  the  significance  of 
the  conditions  here  shown  is  unmistakable.  This  is  not  a  hap- 
hazard process,  observed  only  occasionally,  in  a  limited  number 
of  embryos,  and  then  only  in  single  sections,  or,  at  most,  in  a  few 
successive  sections.  In  any  average  embryo  of  the  proper  age 
the  same  structures  appear  regularly  in  the  same  situations  and 
in  identical  relationship  to  the  embryonic  environment.  It  is 
often  possible,  as  the  microphotographs  and  the  corresponding 


30          DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

reconstructions  herewith  published  clearly  show,  to  trace  the 
forming  lymphatic  with  its  atrophied  vein  kernel  for  long  stretches, 
and  in  different  embryos  of  approximately  the  same  crown-rump 
measure  the  consistent  repetition  of  identical  histological  pictures 
is  remarkable. 

There  are,  of  course,  as  in  the  ontogeny  of  other  structures, 
individual  cases  of  variation  in  which  systemic  lymphatic  develop- 
ment is  either  more  advanced  or  more  retarded  than  is  normal 
for  the  average  of  any  given  stage.  But  if  a  large  number  of 
embryos  of  each  typical  period  are  examined  and  compared,  the 
average  standard  of  extraintimal  lymphatic  development  attained 
by  the  majority  of  individuals  in  each  stage  is  remarkably  con- 
stant and  uniform. 

The  earliest  stage  in  which  I  have  encountered  this  typical 
replacement  of  an  early  embryonic  vein  by  a  perivenous  extrainti- 
mal lymphatic  is  presented  by  certain  12  mm.  cat  embryos  along 
the  caudal  circumference  of  the  azygos-precardinal  confluence. 
In  the  concavity  of  the  azygos  arch  on  each  side,  as  this  vessel 
turns  ventrad  to  join  the  precardinal  vein,  these  earliest  evidences 
of  the  extraintimal  replacement  of  preceding  embryonic  veins 
by  independent  perivenous  lymphatic  spaces  are  encountered. 
Thus,  fig.  10  shows  a  section  of  this  region  in  a  12  mm.  cat 
embryo  (series  217,  slide  x,  section  12).  Here  the  typical  pic- 
ture of  the  central  collapsed  core  of  the  earlier  vein  (Jf),  enveloped 
by  the  clear  extraintimal  lymphatic  space  (5),  is  plainly  to  be  seen. 
Fig.  11  shows  the  same  region  in  another  12  mm.  embryo  (series 
211,  slide  x,  section  15).  Both  the  degenerating  venule  (4) 
and  the  enveloping  lymphatic  (5)  are  larger  than  in  the  pre- 
ceding series,  and  occupy  the  same  position  between  aorta  (7) 
and  left  precardinal  vein  (6). 

In  a  14  mm.  embryo  (series  127,  slide  viii,  section  12,  fig.  12) 
the  section  passing  just  caudad  to  the  junction  of  left  azygos 
(6)  with  left  precardinal  vein  (6}  shows  these  early  lymphatic 
spaces  (5}  and  their  relation  to  the  contained  venous  remnant  (4) 
fully  developed.  Only  one  of  the  areas  is  denoted  by  leaders 
in  the  figure,  but  two  equivalent  areas  are  seen  further  dorsad 
and  nearer  to  the  ventral  aspect  of  the  azygos  arch.  The  lym- 


RELATION  OF  LYMPHATIC  TO  BLOOD- VASCULAR  SYSTEM  31 

phatic  plexus,  as  development  proceeds,  from  the  12  mm.  stage 
on,  approaches  the  large  venous  trunks  more  and  more,  until 
the  spaces  lie  in  direct  apposition  with  the  same,  and  unite  to 
form  the  lymphatic  trunk  eventually  destined  to  replace  the  left 
azygos  arch  and  adjacent  position  of  the  left  precardinal  vein. 
This  trunk  then  constitutes  the  cephalic  end  of  the  broncho- 
mediastinal  duct  (37).  Thus  figs.  13  and  14  show  two  sections 
through  the  same  region  in  a  15  mm.  embryo  (series  219,  slide 
xiv,  sections  19  and  16).  Compared  with  the  14  mm.  embryo 
.the  left  azygos  vein  shows  a  marked  reduction.  The  lym- 
phatic spaces  have  enlarged  and  present  a  clear  lumen  on 
section,  the  remnant  of  the  earlier  vein,  around  which  they 
developed,  having  disappeared.  The  spaces  lie  between  aorta 
and  left  precaval  vein,  in  close  approximation  to  the  dorso-medial 
circumference  of  the  latter.  The  azygos  segment  of  the  thoracic 
duct  (86)  is  seen  dorsal  to  the  interval  between  aorta  and  oesoph- 
agus, and  ventral  to  the  scant  remnants  of  the  earlier  interazygos 
venous  anastomosis  (15). 

The  reconstruction  of  a  15  mm.  embryo  (series  218)  shown  in 
fig.  170  in  Part  II,  gives  a  clear  idea  of  the  extent  and  relations  of 
this  lymphatic  complex  (37)  in  this  stage. 

B.  Partial  replacement  of  portions  of  the  territory  of  an  early 
embryonic  venous  pathway  by  an  extraintimal  lymphatic  vessel,  both 
venous  and  lymphatic  channels  either  persisting  side  by  side  up  to 
later  developmental  periods,  or  forming  correlated  components  of 
the  permanent  adult  vascular  organization. 

The  developmental  processes  just  described  appear  most  clearly 
marked  in  the  earlier  stages,  and  in  connection  with  temporary 
embryonic  channels  and  plexuses  which  are  destined  to  undergo 
rapid  degeneration  and  ultimate  complete  elimination.  In  the 
case  of  the  embryonic  veins  which  are  retained  for  a  longer  period, 
or  carried  over  into  the  permanent  adult  organization,  the  his- 
togenetic  stages  of  lymphatic  development  are  identical  in  kind, 
and  differ  only  in  degree  from  those  just  detailed.  In  place  of 
complete  replacement  of  the  antecedent  vein  by  the  lymphatic 
channel,  this  replacement  is  only  partial  and  leads  to  the  typical 


32         DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

close  parallel  association  of  lymphatic  and  venous  vessels  so 
characteristic  of  the  later  embryonic  stages  and  of  the  per- 
manent adult  pathways  of  both  the  lymphatic  and  the  venous 
systems. 

Figs.  15  and  16  show  transverse  sections  of  a  14  mm.  embryo 
(series  222,  slide  vii,  section  26,  and  slide  viii,  section  4)  in  the 
region  of  the  external  jugular  vein.  The  lymphatic  spaces  (27'} 
are  in  full  development,  and  are  applied  chiefly  to  the  medial 
aspect  of  the  plexus  of  the  external  jugular  vein  (27}.  The  lym- 
phatic endothelium  is  clearly  marked. 

Fig.  17  shows  a  transverse  section  in  the  upper  thoracic  region 
of  another  14  mm.  embryo  (series  37,  slide  xiii,  section  12).  A 
typical  lymphatic  anlage  (53}  is  applied  to  the  medial  wall  of  the 
left  precaval  vein. 

Fig.  18  shows  a  transverse  section  through  the  mid-thoracic 
region  in  a  17  mm.  cat  embryo  (series  258,  slide  xviii,  section 
9,  X225). 

The  extraintimal  anlages  of  the  thoracic  ducts  (36} ,  which  usually 
in  thisstage  have  advanced  to  the  production  of  a  continuous  and 
uninterrupted  channel  system,  are  seen  on  each  side  closely  ap- 
plied to  the  ventral  aspect  of  the  left  and  right  azygos  veins. 
The  latter  are  in  the  height  of  their  development,  forming  large 
and  symmetrical  longitudinal  venous  trunks  (8,  6}  connected  by 
the  supra-aortic  interazygos  anastomosis.  In  course  of  further 
development  the  left  azygos  vein  and  the  interazygos  anastomosis 
are  destined  to  undergo  progressive  reduction  until  they  are 
eventually  entirely  lost.  Their  topographical  position  is  then 
occupied  by  the  replacing  left  segment  of  the  thoracic  duct  com- 
plex (86}.  The  right  azygos  vein,  which  is  carried  as  a  perma- 
nent vessel  into  the  adult  organization,  also  undergoes  consider- 
able relative  reduction,  correlated  to  the  corresponding  increase 
in  the  caliber  of  the  main  (right)  segment  of  this  portion  of  the 
thoracic  duct  complex. 

The  beginning  of  this  process  is  seen  well  in  fig.  19,  which  shows 
a  transection  of  the  same  region  in  a  19  mm.  cat  embryo  (series 
253,  slide  xxiv,  section  9,  X  225).  The  change  from  the  preceding 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM  33 

stage  (fig.  18)  is  marked  both  in  the  venous  and  the  lymphatic 
channels.  The  former  are  relatively  much  reduced,  while  the 
latter  have  correspondingly  increased  in  extent.  The  azygos  is 
mainly  represented  by  the  right  channel  (3} .  The  left  channel  (0) 
has  become  small,  but  is  still  connected  by  the  transverse  inter- 
azygos  anastomosis  (15}  with  the  larger  and  permanent  right 
trunk.  The  right  thoracic  duct  (86}  is  likewise  large.  A  dorso- 
medial  extension  of  the  same,  which  carries  into  the  interval 
between  aorta  and  interazygos  plexus,  will,  in  later  stages,  replace 
the  latter  secondarily,  after  the  complete  recession  of  the  left 
azygos  vein.  The  left  thoracic  duct  (86}  is  also  of  large  size  and 
fills  a  considerable  part  of  the  area  formerly  (fig.  18)  occupied 
by  the  left  azygos  trunk.  Some  decadent  remnants  of  the  ventro- 
medial  azygos  plexus  (4)  are  still  seen  associated  with  the  left 
duct,  and  are  in  process  of  replacement  by  a  lymphatic  space  (5} 
destined  to  make  connection  between  the  left  thoracic  duct  anlage 
and  the  mesenteric  lymphatic  plexuses  (cf.  p.  148,  figs.  266  to 
270,5.7). 

Figs.  20  to  24  show  transverse  sections  in  the  region  of  the  devel- 
oping mesenteric  lymphatics  and  of  the  ascending  lumbar  lym- 
phatic trunks  in  a  17  mm.  embryo  (series  258,  slide  xxiii,  sections 
34,  33,  32  and  31.)  The  embryonic  veins  (74)  occupying  the  root 
of  the  mesentery  caudal  to  the  subcardinal  cross-anastomosis  are 
in  the  process  of  being  replaced  by  extraintimal  lymphatic  spaces 
(51}  which  are  destined  to  become  confluent  and  form  the  anlage 
of  the  future  mesenteric  lymphatic  sac. 

The  region  in  question  is  not  only  interesting  in  reference  to 
the  ontogenesis  of  the  abdominal  lymphatic  sacs  and  channels, 
but  the  arrangement  of  the  periaortic  axial  venous  trunks  and 
their  relation  to  the  developing  lymphatics  is,  in  combination  with 
the  next  following  stage  (20  mm.,  figs.  25  and  26),  of  the  highest 
importance  in  interpreting  the  phylogenetic  relations  of  the  main 
abdominal  veins  in  mammalia.  For  these  reasons  a  somewhat 
more  detailed  consideration  of  the  sections  may  properly  be  in- 
troduced here. 

Fig.  20  shows  section  34  of  slide  xxiii  of  series  258  in  a  magnifica- 
tion of  75  diameters  and  affords  a  comprehensive  picture  of  the  entire 


34        DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

topographical  field  involved.  The  strands  of  the  sympathetic  (l) 
are  supra-aortic.  On  each  side  of  the  aorta  (7)  are  the  large  and  sym- 
metrically developed  right  and  left  postcardinal  veins  (67  and  68} , 
with  the  ascending  trunks  of  the  ilio-lumbar  arteries  (A.ilio-lumb. 
transv.  ant.)  (not  labelled  in  the  figure)  applied  to  their  ventro- 
lateral  circumference.  The  subaortic  area  shows  the  cross-sections 
of  four  symmetrical  vascular  channels,  two  venous  and  two  lym- 
phatic. Immediately  vential  to  the  aorta,  and  closely  applied  to 
its  ventral  wall  and  to  each  other,  are  two  longitudinal  parallel 
axial  veins  which  are  connected  at  intervals  by  a  few  short  trans- 
verse anastomoses.  These  vessels  are  the  temporary  and  very 
evanescent  homologues  in  the  placental  embryo  of  the  channels 
which  McClure30  has  described  as  the  "cardinal  collateral  trunks" 
in  the  embryo  of  Didelphis  marsupialis,  and  from  which  he  has 
traced  the  development  of  the  preaortic  postcava  characteristic 
of  the  Marsupalia.  These  vessels  are  derivatives  from  the  earlier 
preaortic  cardinal-subcardinal  venous  plexus  below  the  cross- 
anastomosis,  but  differentiate  in  Marsupials  along  separate  and 
distinct  axial  lines.  They  are  destined,  as  are  the  corresponding 
portions  of  the  subcardinals  proper,  to  be  entirely  replaced  in  the 
typical  placental  development  by  the  chain  of  preaortic  lymph 
channels  and  nodes,  but  are  capable,  in  aberrant  types  among  the 
placentalia,  of  yielding,  by  further  and  continuous  development, 
a  type  of  preaortic  postcava  which  in  every  respect  corresponds 
to  that  encountered  in  Marsupials.  McClure31  has  described  this 
condition  in  Tragulus,  and  his  observation  has  been  confirmed 
in  a  number  of  dissections  by  Beddard  and  others.  The  fortunate 
acquisition  recently  of  a  series  of  Tragulus  embryos,  through  the 
kindness  of  the  officials  of  the  Smithsonian  Institution,  has  enabled 
my  associate  Tilney  to  trace,  in  a  publication  now  in  preparation 
for  the  press,  the  development  of  the  venous  and  lymphatic 
systems  in  this  aberrant  ungulate  in  their  mutual  interdependence, 
and  to  show  the  correspondence  of  the  venous  genetic  processes 

*°  C.  F.  W.  McClure:  "The  Anatomy  and  Development  of  the  Postcava  in 
Didelphis  marsupialis."  Am.  Jour.  Anat.,  vol.  v,  1906. 

11  C.  F.  W.  McClure:  "The  Postcava  of  an  Adult  Indian  Chevrotain  (Tragulus 
meminna,  Erxleben).  Anat.  Am.,  Band,  xxix  no.  13  and  14,  1906,  pp.  375-377. 


RELATION    OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM         35 

with  those  observed  by  McClure  in  Didelphis.  We  have  here, 
therefore,  an  undoubted  instance  in  which,  in  an  ungulate  placen- 
tal,  the  organization  of  the  abdominal  venous  and  lymphatic  com- 
plex dates  back,  phylogenetically,  to  the  period  of  a  common  mam- 
malian, or  even  amniote,  vascular  groundplan  (text  figure  A,  p. 
41),  forming  the  starting  point  from  which  all  types  of  normal 
and  variant  postcaval  organization,  monotreme,  marsupial  and 
placental,  radiate.  This  makes  it  possible,  as  in  the  ungulate 
genus  just  mentioned,  to  find  in  otherwise  valid  placental  forms, 
as  a  constant  and  normal  structural  character,  the  postrenal 
segment  of  the  postcava  as  a  single  median  preaortic  vessel,  which 
receives,  usually,  both  sex  veins,  and  corresponds  in  every  respect 
to  the  characteristic  marsupial  venous  type.  This  channel  is  the 
final  and  permanent  product  of  the  fusion  of  the  two  embryonal 
cardinal  collateral  veins,  which,  in  the  typical  placental,  either 
do  not  develop  at  all,  as  distinct  veins,  or  else,  as  in  the  cat,  appear 
during  the  ontogenseis  only  for  a  very  short  period,  and  are  sub- 
sequently entirely  replaced  by  extraintimal  lymphatic  spaces 
eventually  uniting  to  form  the  extensive  right  and  left  ascending 
lumbar  lymphatic  trunks.  These  vessels  (75}  are  seen  in  the  prep- 
aration under  discussion  on  each  side,  ventro-lateral  of  the  aorta 
in  the  space  between  the  postcardinal  veins  (67  and  68)  and  the 
cardinal  collateral  veins  (74).  These  large  lymphatic  channels 
have  been  developed  through  the  fusion  of  numerous  separate 
extraintimal  spaces  surrounding  and  finally  replacing  some  of  the 
elements  of  the  earlier  preaortic  venous  plexuses.  A  condensed 
portion  of  the  latter  still  persists  in  this  embryo  as  the  cardinal 
collateral  veins  (7Jf)  above  referred  to.  Eventually  these  also 
are  destined  to  undergo,  in  course  of  normal  development,  complete 
extraintimal  replacement  by  lymphatic  channels.  These  latter 
thus  come  to  occupy  in  the  typical  placental  secondarily  the  ter- 
ritory which  in  monotremes,  marsupials  and  atypical  placentalia 
(Tragulus)  is  filled  by  the  postrenal  preaortic  postcava  (cardinal 
collateral). 

It  is  interesting  to  note  in  this  connection  that  a  detailed  exami- 
nation of  over  900  adult  cats  failed  to  reveal  a  single  instance  in 
which  the  postrenal  segment  of  the  postcava  was  formed  through 


36    DEVELOPMENT  OF  THE  SYSTEMIC  LYMPHATIC  VESSELS 

persistence  and  further  development  of  the  cardinal  collateral 
veins.  In  other  words,  not  a  single  individual  in  the  entire  series 
possessed  a  marsupial  postcava,  although  every  shade  in  the  possi- 
ble range  of  variation  in  the  district  of  the  post-  and  supracardinal 
lines  was  represented  by  numerous  examples.  Thus  with  an  ab- 
dominal venous  organization  of  very  unstable  equilibrium,  as  shown 
by  the  large  percentage  of  cardinal  variants,24  the  cat  yet  keeps 
entirely  within  the  district  of  the  common  genetic  ground  plan 
assigned  to  the  placentalia.  This  phylogenetic  consistency  is 
maintained  in  spite  of  the  fact  that,  as  just  demonstrated  in  series 
258,  the  embryo  develops  the  raw  materials,  as  cardinal  collateral 
channels,  out  of  which  a  preaortic  postcava  of  the  marsupial 
type  could  be  evolved.  In  my  own  estimation  cats  possessing  this 
form  of  postcava  may  exist  and  may  eventually  be  found.  But 
the  failure  to  encounter  them  in  the  relatively  large  series  of  adults 
already  examined  speaks  volumes  for  the  value  of  vascular  organ- 
ization in  interpreting  phylogenetic  relations. 

In  this  light  the  postcaval  development  and  adult  structure  of 
Tragulus,  for  example,  are  of  the  utmost  importance  and  signifi- 
cance. The  unprejudiced  observer  is  often  forced  to  wonder 
why  some  exponents  of  palaeontological  research  are  content  to 
draw  far-reaching  phylogenetic  conclusions  from  the  remnants  of 
the  incomplete  locomotory  apparatus  at  their  disposal,  without 
utilizing  the  results  of  modern  comparative  anatomical  and  embryo- 
logical  investigation  in  determining  at  least  the  mutual  relations 
of  the  extant  forms,  massed  by  an  ironclad  taxonomy  into  more 
or  less  questionable  groups,  whose  ancestry  and  derivation  form 
one  of  the  primary  problems  of  the  palaeontologist.  The  case  of 
Tragulus  just  alluded  to,  the  parotid  complex  and  alimentary 
canal  of  Hyrax,  the  amniote  homologies  of  the  derivatives  of  the 
Sulcus  buccalis  determined  by  Schulte,  the  sharp  line  of  lymphatic 
demarcation  recently  shown  by  Silvester  to  structurally  separate 
absolutely  the  platyrrhine  and  catarrhine  divisions  of  the  lower 
primates,  these  and  other  facts  are  only  instances  in  which  the 
inadequacy  of  a  superficial  convergence  of  dental  and  skeletal 
characters,  for  the  purpose  of  establishing  valid  phylogenetic 
relations,  is  revealed  by  cardinal  divergence  in  the  far  more  stable 
and  important  organization  of  vascular  and  visceral  structure 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          37 

The  prevalent  lack  of  coordinate  deduction  between  verte- 
brate morphology  and  palaeontology  is  accentuated 'by  contrast 
with  such  publications  as  Weber's  "  Saugethiere "  and,  more 
recently,  W.  K.  Gregory's  "The  Orders  of  Mammals",  based 
largely  on  the  author's  joint  work  with  Osborn,  and  on  the  latter's 
previous  classical  researches,  and  published  by  the  American 
Museum  of  Natural  History  (Bulletin,  vol.  27,  February,  1910). 

Workers  in  the  general  field  of  vertebrate  structure  appreciate 
fully  the  immense  practical  value  in  their  own  special  investi- 
gations of  books  of  this  type,  in  which,  to  quote  Gregory's  words, 
"the  data  of  systematic  mammology,  of  comparative  anatomy 
and  embryology  shall  ultimately  be  integrated  with  the  data  of  pal- 
aeontology, to  the  great  advantage  of  these  now  more  or  less 
independent  lines  of  study." 

In  embryo  258  (fig.  21)  the  space  ventral  to  the  cardinal  col- 
lateral veins  and  the  ascending  lumbar  lymphatic  trunks,  is  oc- 
cupied by  a  plexus  of  mesenteric  lymphatics  (51}  draining  into 
the  latter.  On  each  side  are  seen  sections  of  the  ureter  (58},  and 
further  laterad  of  the  iliac  vessels  (61}.  Ventral  of  the  intestine 
(62}  are  the  Wolffian  ducts  (64)  and  the  cloaca  (63} ,  with  the 
hypogastric  arteries  (66}  laterally. 

Fig.  21  shows  the  important  central  vascular  region  of  the  same 
section  in  a  magnification  of  150  diameters.  The  relation  of  the 
cardinal  collateral  trunks  (74)  to  the  ascending  lumbar  lymphatics 
(75),  and  of  the  latter  to  the  postcardinal  veins  (67,  68}  can  be 
more  clearly  seen.  The  lumen  of  the  mesenteric  lymphatics 
(51}  still  contains  in  places  remnants  of  the  decadent  venous 
plexus  around  and  upon  which  they  developed  as  replacing  ex- 
traintimal  spaces. 

The  three  succeeding  sections,  tracing  the  structures  caudo- 
cephalad,  are  shown  in  figs.  22,  23  and  24,  all  in  a  magnification 
of  150  diameters.  The  connections  of  the  lymphatic  channels 
developing  along  the  iliac  vessels  with  the  ascending  lumbar 
trunks  are  especially  well  seen  on  the  left  side  of  the  three  figures, 
also  the  anastomoses  between  the  two  cardinal  collateral  veins  in 
figs.  23  and  24. 

Figs.  25  and  26  show  transverse  sections  of  the  hinder  end  of  the 
body  in  a  20  mm.  embryo  (series  241). 


38         DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC   VESSELS 

Fig.  25  (series  241,  slide  xxx,  section  4)  gives,  in  a  magnifi- 
cation of  75  diameters,  a  topographical  view  of  the  entire  field. 
This  stage,  compared  with  the  preceding  17mm.  embryo,  is  marked 
by  the  full  development  of  the  supracardinal  venous  line,  respon- 
sible for  the  production  of  the  greater  portion  of  the  typical 
adult  placental  postcava  below  the  renal  level,  and  by  the  cor- 
related development  of  the  supra-  or  retro-aortic  lymphatic 
sinuses  associated  with  the  same. 

The  periaortic  area  in  fig.  25  gives  a  clear  view  of  the  vascular 
relations  and  of  the  postcardinal  and  supracardinal  axial  venous 
trunks. 

The  former  (67,  68,}  are  seen  on  each  side,  between  aorta  (7) 
and  metanephros  (65),  receiving  the  veins  from  the  mesonephroi 
in  whose  dorso-medial  border  they  are  lodged. 

The  latter  (59,  60)  lie  dorsal  to  the  aorta  (7)  between  this  ves- 
sel and  the  sympathetic  strands  (1). 

The  right  supracardinal  (60)  has  already  gained  the  ascendency 
and  is  in  process  of  establishing  the  channel  of  a  normal  right 
retro-aortic  postcava,  which  is  the  typical  vein  for  the  cat.  The 
correspondingly  reduced  left  supracardinal  (59)  occupies  the  same 
situation  on  the  left  side.  Associated  with  the  supracardinal 
venous  channels  are  the  supracardinal  lymphatic  trunks  (76), 
which  form  the  anlages  of  the  main  adult  retro-aortic  lymphatic 
plexus.  These  develop  as  extraintimal  spaces  replacing  portions 
of  the  earlier  supracardinal  venous  reticulum.  In  accordance 
with  the  normal  type  of  development  observed  in  this  individual 
embryo,  the  large  permanent  supracardinal  (postcaval)  vein  of 
the  right  side  is  accompanied  by  a  relatively  small  lymphatic 
channel  (76  right),  while  on  the  left  side  the  much  reduced  left 
supracardinal  (59)  is  already  nearly  replaced  by  the  correspond- 
ing lymphatic  vessel  (76  left).  In  course  of  further  normal  devel- 
opment this  replacement  will  become  complete  and  then  the 
area  formerly  occupied  by  the  left  supracardinal  vein  will  be 
entirely  filled  by  the  substituted  large  left  retro-aortic  lymphatic. 
The  permanent  functional  venous  channel  of  the  right  side  (60) 
on  the  other  hand,  developing  into  the  typical  placental  post- 
cava, will  be  accompanied  by  a  relatively  small  right  lymphatic 


DELATION    OF   LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          39 

trunk  following  its  dorso-lateral  aspect.  As  will  be  shown  later 
(PartV.),  departures  from  the  normal  type  of  venous  develop- 
ment in  this  region,  and  the  substitution  of  other  embryonic 
pathways  for  the  right  supracardinal  in  building  up  this  section 
of  the  adult  postcava,  produce  corresponding  and  correlated 
changes  in  the  arrangement  of  the  main  retro-aortic  lymphatic 
channels. 

Fig.  26  shows  the  periaortic  region  of  the  same  embryo,  further 
caudad,  in  a  magnification  of  150  diameters  (series  241,  slide 
xxx,  section  14.)  The  section  is  taken  at  the  level  of  a  pair  of 
dorsal  intersegmental  arteries  which  pierce  the  supracardinal 
venous  (59,  60)  and  lymphatic  (76)  complex,  and  divide  the  vein 
of  the  right  side  into  two  components  (60,  60).  Further  ventrad 
the  two  postcardinal  veins  (67,  68)  are  seen,  already  consider- 
ably reduced,  ventrolaterad  to  the  ureters  (58)  and  the  accom- 
panying ascending' lumbar  lymphatic  trunks  (75).  The  connec- 
tion of  the  latter  with  the  supracardinal  lymphatic  channel  is 
especially  clear  on  the  right  side  of  the  embryo. 

Taken  together,  the  17  mm.  and  20  mm.  embryos  just  figured 
and  described  afford  a  very  clear  and  comprehensive  picture  of 
venous  and  lymphatic  development  in  their  mutual  relationship 
in  this  region. 

The  schematic  text  figures  A,  B  and  C  may  help  to  explain 
this  relationship. 

Fig.  A  is  based  on  the  joint  studies  which  McClure  and  I  made 
on  the  development  of  the  postcava  in  embryos  of  the  domestic 
cat.  The  figure  was  demonstrated  to  the  21st  Session  of  the 
Association  of  American  Anatomists  in  1906  at  the  time  of  pre- 
sentation of  the  communications,  although  not  reproduced  in  the 
brief  abstracts  of  the  papers  subsequently  published.23' 25 

The  figure  represents  a  composite  schema  of  the  main  peri- 
aortic  venous  axial  pathways  of  the  abdominal  region.  These 
pathways  developing  along  definite  and  constant  axial  hydro- 
static lines  out  of  the  periaortic  venous  reticulum,.have  all  been 
determined  by  us  in  embryos  of  the  cat.  They  do  not,  of  course, 
all  coexist  at  the  same  time  in  any  embryonic  stage,  but  normally 
succeed  each  other  in  definite  sequence.  The  entire  range  of 


40          DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

extensive  variations  in  the  domain  of  the  adult  postcava  of  the 
cat  can  be  clearly  interpreted  genetically25  on  the  basis  of 
this  common  groundplan,  through  abnormal  persistence  of  one 
or  more  of  the  embryonal  pathways  usually  destined  for  complete 
obliteration,  thus  producing  farreaching  modifications  in  the 
structure  and  relations  of  the  resulting  atypical  postrenal  seg- 
ment of  the  adult  postcava. 

This  periaortic  axial  venous  lattice  with  connecting  trans- 
verse branches  (Fig.  A)  contains  four  components  on  each  side , 
which  develop  in  the  following  order  : 

1 .  The  postcardinal  veins  (1 ) . 

2.  The  subcardinal  veins  (2}. 

3.  As  secondary  derivatives  of  these  two  veins,  the  preaortic 
cardinal  collateral  channels  (3). 

4.  As  secondary  dorsal  derivatives  of  the  postcardinal  trunks, 
the  supracardinal  veins  (4).  • 

In  the  course  of  normal  venous  development  along  the  line 
typical  for  the  great  majority  of  placental  mammals  the  right 
supracardinal  vein  (4)  obtains  the  preponderance  and  furnishes 
the  postrenal  segment  of  the  adult  postcava,  thus  freeirg  the 
ureter  from  its  primitive  retro-venous  position. 

A  part  of  the  early  capillary  periaortic  reticulum,  out  of  which 
this  vessel  develops,  is  secondarily  replaced  by  extraintimal 
lymphatic  spaces,  which  through  their  confluence  form  the  rela- 
tively small  retro-aortic  lymph  channel  (4'),  folio  wing  in  the  adult 
the  dorso-lateral  circumference  of  the  postcava  (4).  (Figs.  B  and 
C). 

The  right  and  left  postcardinal  veins  (1}  are  in  part  retained 
as  the  terminals  of  the  sex  veins,  in  part  replaced  by  the  accom- 
panying lymphatic  trunks  (!'}.  (Figs.  B  and  C). 

The  left  supracardinal  vein  (4),  and  both  subcardii^,1  veins 
(2},  below  the  cross-anastomosis,  as  well  as  both  cardinal  collat- 
eral veins  (3),  retrograde  and  are  entirely  replaced  secondarily 
by  lymphatic  channels. 

The  lymphatic  replacing  the  left  supracardinal  vein  (4  )  forms 
normally  in  the  adult  the  main  retro-aortic  lymphatic  sinus. 
(4',  lef  t,  in  figs.  Band  C). 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM         41 


"\ 


Monotreme 


Ureltei 


Sex  vei 


Sex  vein 


42         DEVELOPMENT  OF   THE    SYSTEMIC   LYMPHATIC   VESSELS 

The  lymphatic  channels  replacing  the  subcardinal  and  cardinal 
collateral  venous  trunks  form  the  extensive  system  of  the  adult 
ascending  lumbar  and  preaortic  lymphatic  vessels  and  nodes 
(2f  and  3'  in  figs.  B  and  C). 

Of  course  it  is  quite  apparent  that  the  adult  placental  differ- 
entiation occurs  in  the  district  of  the  post-  and  supracardinal 
lines,  with  a  strong  predilection  for  the  right  supracardinal  as 
the  main  path  of  the  postrenal  segment  of  the  adult  postcava. 
It  is  equally  apparent  that  in  correctly  valuing  the  significance 
of  the  departures  from  the  normal  type  of  placental  postcava 
all  four  of  the  available  components,  viz.,  right  and  left  post- 
cardinal  and  right  and  left  supracardinal  lines,  must  be  taken 
into  account  as  potential  factors  in  the  development  of  the  atyp- 
ical placental  postcava.  The  relation  of  the  veins  to  the  ureter 
will  then  decide  the  question  of  the  genetic  derivation,  as  being 
either  the  persistent  postcardinal  or  supracardinal  channel  of  either 
the  right  or  left  sides,  in  the  case  of  single  trunks,  or  of  both  sides 
in  instances  of  double  bilateral  adult  channels. 

Thus  all  the  recorded  cases  of  variant  postcaval  veins  of  the 
cat,  and  of  man,  can  be  clearly  interpreted  on  this  basis,  as  has 
been  done  by  McClure,  Darrach  and  myself  in  previous  publi- 
cations.23'24'25 

Furthermore,  the  placental  types  in  which  a  normally  so-called 
double  postcaval  vein  occurs,  as,  e.g.  in  some  of  the  aquatic 
carnivores,  some  insectivores  and  edentates,  are  readily  led  back 
to  persistence  of  both  right  and  left  axial  channels  with  absence 
or  reduction  of  the  iliac  anastomosis.  Again  the  position  of  the 
ureter  in  reference  to  the  bilateral  trunks  will  characterize  each 
of  them  as  being  either  post-  or  supracardinal  in  derivation. 

In  the  marsupials  McClure's  researches  already  quoted,31 
show  clearly  that  the  members  of  this  subclass  depend  upon  the 
continued  development  of  the  ventral  preaortic  venous  path- 
ways (2,  3}  of  the  common  vertebrate  groundplan  (fig.  A)  for 
the  evolution  of  their  typical  ventral  preaortic  postrenal  seg- 
ment of  the  postcava,  with  consequent  reduction  of  the  post- 
cardinal  line  (.7)  to  the  role  of  a  sex  vein  terminal,  and  the  complete 
suppression  of  the  typical  placental  supracardinal  lines  (4)  in  most 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          43 

forms,  while  rudiments  of  the  same  are  found,  as  shown  by 
Schulte's  and  Tilney's  observations,  in  connection  with  the  venous 
return  along  the  caudal  vein  only  in  the  Macropodidae.29 

Schulte's  work  on  the  venous  organization  of  the  Monotre- 
mes32  proves,  I  think,  conclusively  the  phylogenetic  value  of  the 
periaortic  venous  reticulum  with  axial  pathways  of  hydrostatic 
selection  which  the  detailed  study  of  placental  embryos  establish. 
His  dissections  of  both  Platypus  and  Echidna  revealed  for  the 
first  time  the  persistence  in  the  Monotreme  of  both  dorsal  supra- 
cardinal  channels,  and  of  ventral  preaortic  vessels  of  subcardinal 
and  cardinal  collateral  derivation,  while,  as  appears  uniformly 
throughout  the  mammalian  class,  the  primitive  postcardinals 
retain  normally  solely  the  function  of  venous  drainage  for  the 
gonad. 

The  facts  just  stated  have  been  in  a  large  part  already  pub- 
lished in  outline  by  McClure,  Schulte,  Tilney,  Darrach  and 
myself.  I  hope  it  will  be  possible  to  collect  the  numerous  obser- 
vations, with  adequate  illustrations,  in  a  publication  to  be  issued 
in  the  near  future.  I  have  recorded  some  of  the  results  obtained 
through  these  joint  investigations  in  this  paper  in  order  to  use 
them  for  the  purpose  of  clearly  outlining  on  a  broad  basis  the 
genetic  possibilities  in  the  development  of  the  venous  system, 
and  the  correlated  interdependence  of  the  systemic  lymphatic 
vessels.  The  latter  will,  in  the  mammal,  take  over  and  further 
develop  territory  formerly  occupied  by  transient  embryonic 
venous  channels,  which  they  secondarily  replace  through  extra- 
intimal  development.  Hence  the  resulting  mirror  picture  which 
the  lymphatic  system  of  the  adult  mammal  presents  in  reference 
to  the  axial  venous  trunks,  whatever  type  of  central  venous  organ- 
ization may  obtain  in  any  individual  instance. 

The  examples  just  given  could,  df  course,  be  indefinitely  multi- 
plied. They  all  show  absolutely  congruent,  uniform  and  constant 
pictures  in  all  parts  of  the  body  of  the  developing  lymphatic  chan- 
nels in  close  association  with  the  adjacent  veins,  but  not  connected 

32  H.  v.  W.  Schulte:  "The  Range  of  Variations  in  Monotremes  and  Australian 
Marsupials."  Anat.  Rec.,  no.  3,  April  1,  1907.  Am.  Jour.  Anat.,  vol.  vi,  no. 
3,  1907. 


44        DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC   VESSELS 

with  the  same.  Nowhere  is  there  any  suggestion  of  a  bud  or  an 
outgrowth  from  the  vein  as  forming  the  origin  of  these  lymphatic 
spaces.  It  now  remains  to  clearly  prove  the  genesis  of  these 
spaces,  and  to  trace  their  growth  from  their  inception  up  to  the 
stages  just  pictured  in  which  fully  organized  lymphatic  and  ve- 
nous channels  lie  side  by  side  in  the  mutual  relation  above  fig- 
ured and  described.  The  proof  of  their  origin  is  furnished  by  the 
series  of  microphotographs  of  successive  sections  of  the  earlier 
stages  given  in  Part  II  of  this  communication,  in  connection  with 
the  individual  series  described  and  figured  in  tracing  the  develop- 
ment of  the  preazygos  and  azygos  portions  of  the  thoracic  ducts. 
The  microphotographs,  and  especially  the  reduced  reproductions 
figured,  are  not  so  clear  as  the  actual  preparations,  because  focal 
adjustment  is  required  to  follow  the  endothelial  lining  of  the 
spaces  in  their  entire  circumference,  and  because  they  lack  the 
differential  stain  of  the  sections.  Still  they  are  sufficiently  dis- 
tinct to  establish  definite  conclusions.  Merely  referring,  there- 
fore, at  this  time  to  the  following  detailed  illustrations,  the  general 
topic  of  extraintimal  replacement  of  embryonic  veins  by  lym- 
phatic spaces  and  the  character  of  the  latter  deserve  some  further 
consideration. 

The  lymphatic  anlages,  as  above  stated,  if  studied  under  suffi- 
ciently high  power  and  with  some  care,  are  seen  to  begin  as  inter- 
cellular clefts  in  the  periaortic  mesoderm,  adjacent  to  the  postcar- 
dinal  venous  plexus,  and  chiefly  on  its  ental  aspect,  between  it  and 
the  aorta. 

The  individual  lymphatic  spaces,  at  first  small  and  separated 
from  each  other,  enlarge,  elongate  and  become  confluent,  to  form 
larger  continuous  channel  segments,  while  innumerable  newly 
formed  spaces  of  the  same  character  appear  in  the  surrounding 
tissue,  join  with  each  other,  and  with  the  earlier  preformed  lym- 
phatic channels,  in  exactly  the  same  manner,  and  with  the  same 
appearance  of  lymph  endothelial  "budding"  or  " sprouting"  as 
is  observed  in  haemal  vascularization  of  new  areas  by  the  junction 
of  the  earlier  blood  capillary  anlages  with  secondary  haemal 
plexuses.  In  these  later  stages  the  veins  are  surrounded  by  a  close 
lymphatic  plexus,  which,  however,  does  not  as  yet  form  a  con- 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          45 

nected  channel  system,  but  is  composed  of  longer  and  shorter 
segments  still  independent  of  each  other. 

These  finally  become  confluent,  to  form  the  main  systemic 
lymphatic  collecting  trunks,  and  then  only  do  these  establish 
their  final  junction  with  the  jugular  lymph  sacs,  through  whose 
interposition,  as  above  stated,  they  gain  in  the  typical  mammal 
their  permanent  entry  into  the  venous  system. 

In  this  ontogenesis  of  the  systemic  lymphatic  vessels  certain 
relations  between  them  and  the  venous  system  deserve  further 
notice. 

In  the  early  stages  the  lymphatic  mesenchymal  spaces  form  a 
wide  meshed  network  (cf.  series  111,  figs.  1  to  7,  series  120,  figs. 
8  and  9).  There  is  thus  a  marked  similarity  in  the  earliest  stages 
of  both  the  haemal  and  the  lymphatic  vessels,  for  the  peripheral 
venous  embryonic  pathways  are  in  their  corresponding  stages  like- 
wise still  largely  in  the  condition  of  a  capillary  reticulum.  As  the 
main  lines  of  venous  drainage  crystallize  out  of  the  antecedent 
plexiform  arrangement,  the  adjacent  enlarging  lymphatic  channels 
crowd  in  on  the  condensing  venous  line  and  continue  the  close  re- 
lationship which  the  earliest  lymphatic  anlages  maintain  to  the 
adjacent  veins.  Thus  the  main  embryonic  venous  channels  de- 
velop along  certain  definite  hydrostatic  lines  by  enlargement  and 
confluence  of  the  individual  plexiform  elements  of  the  indefinite 
antecedent  network  occupying  these  lines.  The  capillaries  out- 
side of  these  lines  retrograde,  so  that  the  area  of  crosssection  of 
the  defined  venous  channel  is  less  than  the  cross-cut  area  of  the 
plexiform  network  which  it  replaces.29 

The  distinct  impression  is  given  that  the  space  thus  vacated 
by  the  condensation  of  the  plexiform  venous  network  of  the  ear- 
lier stages  affords  to  the  replacing  lymphatic  plexus  the  oppor- 
tunity for  greater  growth  and  expansion,  and  that  subsequently, 
in  repetition  of  the  process  previously  active  in  the  venous  reticu- 
lum, the  lymphatic  network  condenses  in  a  similar  manner  into 
more  defined  channels  along  similar  hydrostatic  drainage  lines,  so 
that  the  newly  established  main  lymphatic  vessel  now  closely 
follows  the  main  venous  channel.  It  is  to  be  noted,  however, 
that  this  organization  of  main  vascular  channels  is  usually  less 


46         DEVELOPMENT   OF   THE    SYSTEMIC   LYMPHATIC   VESSELS 

complete  in  case  of  the  lymphatic  vessels,  as  compared  with  the 
corresponding  vein.  The  lymphatic  system  retains,  much  more 
perfectly  than  the  venous,  in  many  situations  the  original  embry- 
onic plexiform  type. 

At  first  the  cells  limiting  the  earliest  lymphatic  spaces  are  of 
the  usual  irregular  cuboidal  form.  As  the  spaces  enlarge,  open 
out  and  thus  become  better  defined,  the  limiting  mesodermal  cells 
become  flattened,  and  finally  assume  a  typical  endothelial  char- 
acter and  form.  Thus,  for  example,  the  endothelial  lining  of  the 
primitive  mesodermal  lymphatic  spaces  (77)  is  more  clearly  devel- 
oped in  the  10  mm.  embryo,  series  120,  shown  in  figs.  8  and  9, 
than  in  the  corresponding  sections  of  embryo  111,  of  the  same 
crown-rump  measure  (figs.  1  to  7).  The  former  embryo  is  slightly 
in  advance  of  the  latter  as  regards  the  development  of  the  parie- 
tal endothelial  lining  of  the  primitive  mesodermal  intercellular 
lymphatic  spaces.  In  some  instances  a  few  modified  mesodermal 
cells  intervene  between  the  cells  limiting  the  lymphatic  spaces 
and  the  endothelium  of  the  adjacent  venous  radicle.  In  others 
no  such  intervening  cell-layer  exists,  and  the  lymphatic  space  is 
separated  from  the  venous  lumen  only  by  the  latter 's  endothelial 
wall.  In  other  words,  in  the  extent  of  the  lymphatic  anlage,  a 
single-celled  membrane  furnishes  a  part  of  the  venous  intima  and 
at  the  same  time  contributes  to  the  endothelial  definition  of  the 
lymphatic  space.  This  relation  of  vein  and  lymphatic  anlage  is 
shown  very  clearly  in  fig.  17.  The  lymphatic  space  (53),  which  is 
closely  applied  to  the  medial  wall  of  the  left  precardinal  vein,  is 
only  separated  from  the  lumen  of  the  latter  by  the  endothelial 
membrane  which  serves  to  line  both  spaces  for  the  area  of  their 
mutual  contact  in  this  stage.  Subsequently,  with  the  regression 
of  the  left  precardinal  vein,  this  lymphatic  anlage  will  correspond- 
ingly enlarge  to  form  an  extensive  lymphatic  plexus,  which  will 
eventually  topographically  replace  the  vein  along  which  it  arose. 
In  order  to  briefly  characterize  this  relation  between  vein  and 
lymphatic,  McClure  and  I  defined  in  an  earlier  publication21  these 
spaces  as  the  "Extra-intimal"  anlages  of  the  systemic  lymphatic 
vessels,  with  due  regard  to  the  relation  existing  between  them  and 
the  intimal endothelial  lining  of  the  embryonic  veins.  Themechan- 


RELATION  OF  LYMPHATIC  TO  BLOOD- VASCULAR  SYSTEM  47 

ical  concept  involved  in  this  term  seems,  to  judge  from  a  recent 
publication,33  to  have  been  difficult  to  acquire.  I  am  glad  to  be 
able  to  make  myself  clear  by  reference  to  fig.  17,  where  the  mutual 
relation  of  the  two  vascular  lumina  is  evident  without  further 
description,  and  to  the  numerous  detailed  illustrations  on  a  larger 
scale  of  magnification  which  accompany  the  account  of  the  devel- 
opment of  the  thoracic  ducts  in  Part  II  of  this  communication. 

By  far  the  larger  number  of  the  early  lymphatic  channels  are 
the  product  of  fusion  of  these  "  extra-intimal "  spaces,  and  hence 
closely  follow  the  veins  of  their  respective  regions.  Subsequently, 
with  the  development  of  a  venous  adventitia,  this  relationship 
is  somewhat  altered  in  case  of  those  veins  which  are  included  in 
the  permanent  venous  organization.  The  close  relation  existing, 
however,  throughout  life  between  these  veins  and  the  accompany- 
ing lymphatics  is  based  on  this  intimate  primitive  association  of 
their  respective  anlages. 

On  the  other  hand,  the  extra-intimal  position  of  the  earliest 
lymphatic  spaces  furnishes  the  explanation  of  another  relation 
manifested  between  the  developing  systemic  lymphatic  channels 
and  those  embryonic  veins  which  in  course  of  normal  venous  devel- 
opment are  destined  to  undergo  reduction  and  finally  complete 
suppression,  when  the  primitive  bilateral  and  symmetrical  venous 
system  of  the  earlier  embryonic  stages  shifts  to  the  dextral  as- 
symmetrical  type  of  the  main  adult  axial  channels.  In  these 
circumstances  the  systemic  lymphatic  vessel  associated  with  the 
temporary  embryonic  vein  experiences,  apparently  through  the 
shrinkage  of  the  latter,  an  impetus  to  its  own  more  extensive  de- 
velopment, so  that  it  comes  to  occupy  in  general  topographically 
the  space  filled  by  the  vein  in  the  earlier  stages. 

Thus  the  embryonic  period  which  marks  the  normal  ontogenetic 
swing  of  the  main  venous  line  to  the  right  through  the  secondary 
sinistro-dextral  iliac,  hemiazygos  and  brachiocephalic  cross  anas- 
tomoses, sees  the  simultaneous  increase  in  the  corresponding  lym- 
phatic channels  of  the  left  side,  which  topographically  replace  the 
abandoned  left  embryonic  venous  pathways  of  the  earlier  and  sym- 

33  Sabin:  Anat.  Rec.,  vol.  ii,  1908,  p.  50. 


48      DEVELOPMENT   OF    THE    SYSTEMIC    LYMPHATIC   VESSELS 

metrical  stage.  This  occurrence  leads  to  the  well-known  relative 
location  of  the  main  axial  veins  and  lymphatics  in  the  normal 
adult,  in  which  the  lymphatic  vessels  are  chiefly  situated  on  the 
left  side  and  form,  so  to  speak,  a  mirror-picture  of  the  right  sided 
axial  venous  channels. 

Fig.  27  shows  the  reconstruction  of  the  anterior  venous  and 
lymphatic  complex  in  a  cat  embryo  of  18  mm.  (series  88)  in  the 
ventral  view,  and  fig.  28  of  the  same  preparation  in  the  lateral 
aspect  from  the  left  side.  The  brachiocephalic  cross  anastomosis 
is  already  well  under  way,  resulting  in  a  marked  diminution  of 
the  left  anterior  caval  vessel  and  a  corresponding  increase  in  the 
permanent  right  anterior  cava  or  right  duct  of  Cuvier.  Con- 
versely, the  lymphatic  vessel  accompanying  the  diminishing  left 
precaval  vein  is  of  large  size,  while  that  applied  to  the  massive 
right  precaval  is  comparatively  small. 

This  principle  of  lymphatico-venous  replacement,  indicated 
clearly  in  the  later  embryonic  stages,  is  strikingly  illustrated  in 
the  adult.  Thus,  for  example,  the  adult  cat  presents  normally 
the  arrangement  of  the  great  veins  of  the  head  and  neck  which 
is  so  frequently  encountered  in  mammals  below  Primates,  in 
which  the  large  embryonic  internal  jugular  vein  is  much  reduced 
or  even  entirely  obliterated,  while  secondarily  the  external  jugu- 
lar vein  has  assumed  the  function  of  the  main  vessel.  Under 
these  normal  circumstances  the  lymphatic  trunk  accompanying 
the  minute  internal  jugular  vein  or,  in  case  of  its  entire  default, 
occupying  its  position,  is  well  developed  and  the  largest  element 
of  the  entire  cervical  lymphatic  complex,  while  the  external  jugu- 
lar vein  is,  on  the  other  hand,  accompanied  usually  by  two  very 
slender  lymphatic  vessels. 

In  instances,  however,  in  which  the  embryonic  proportion 
between  the  two  jugular  veins  is  retained  in  the  adult,  so  that  the 
internal  jugular  appears  as  a  large  and  functionally  important 
vessel,  while  the  external  is  correspondingly  diminished,  the  inter- 
nal jugular  lymphatic  trunk  is  reduced,  while  the  double  lymphatic 
vessel  along  the  external  jugular  is  enlarged,  and  evidently  acts 
in  compensation  in  the  cervical  lymphatic  return. 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          49 

Again,  in  the  same  way,  in  adult  animals  with  normally  placed 
right  postcava,  the  main  supracardinal  lymphatic  trunk,  draining 
the  abdomen  and  the  posterior  extremities,  follows  the  left  side  of 
the  large  artery. 

In  the  not  infrequent  instances,  however,  of  left  sided  postcava 
or  postcardinal  vein  in  the  adult  the  reverse  obtains,  and  the  peri- 
aortic  lymphatic  channels  predominate  on  the  right  side  and  oc- 
cupy the  place  usually  filled  by  the  large  vein  in  normal  venous 
development. 

I  have  encountered  in  the  adult  series  so  far  examined  no  in- 
stance of  persistent  left  precava  replacing  functionally  the  normal 
right  superior  cava,  but  have  no  doubt  that  this  venous  variation 
would  involve  a  transposition  of  the  proximal  end  of  the  thoracic 
duct  to  the  right  side,  or  at  least  a  marked  increase  in  the  size  and 
functional  importance  of  the  usually  insignificant  preazygos  seg- 
ment of  the  adult  right  lymphatic  duct. 

The  developmental  outline  just  given  describes  the  mutual 
ontogenetic  relations  of  the  venous  and  lymphatic  systems  through- 
out the  greater  part  of  the  body. 

Systemic  lymphatic  development  in  these  regions  is,  however, 
by  no  menas  confined  to  the  immediate  environment  of  degener- 
ating embryonic  veins.  The  same  field,  which  shows  the  above 
described  histogenetic  processes  in  the  development  of  extrain- 
timal  lymphatic  spaces  surrounding  and  replacing  a  decadent 
venule,  will  at  the  same  time  contain  numerous  equivalent  lym- 
phatic mesenchymal  clefts  and  spaces  which  continue  to  develop 
independently  of  any  association  with  retrograding  veins.  Nat- 
urally, these  independently  developed  early  lymphatic  anlages 
are  less  striking  than  those  above  described  as  developing  in  as- 
sociation with  a  receding  vein.  They  are  smaller,  because  they 
lack  the  bulk  of  the  contained  venous  core,  and  they  are  more 
difficult  to  clearly  differentiate  against  the  surrounding  mesen- 
chyme.  They  are,  however,  always  present  and  their  eventual 
connection  with  the  larger  perivenous  lymphatic  spaces  can  be 
ascertained  definitely  by  following  their  development  through 
the  proper  stages. 


50          DEVELOPMENT   OF   THE    SYSTEMIC     LYMPHATIC   "VESSELS 

In  addition,  in  certain  areas,  a  small  group  of  the  earliest  lym- 
phatic anlages  appear  to  develop  in  the  mesenchyme  along  defi- 
nite lines,  and  in  distinct  patterns,  but  without  any  preceding 
venous  reticulum.  They  impress  me,  for  example,  in  the  area 
surrounding  the  omphalomesenteric  artery,  as  systemic  lymphatic 
channels  developing  ia  the  placental  embryo  in  regions  which  are 
no  longer  ontogenetically  the  seat  of  venous  development,  al- 
though occupied  by  vei.is  in  other  mammalian  types.  Thus  the 
cardinal  collateral  line  of  the  marsupials"  and  the  correlated 
venous  area  of  the  monotremes32  no  longer  develops  as  a  perma- 
nent veoous  plexus  in  placentalia34  but  only  partially  appears 
in  certain  forms  as  a  temporary  and  evanescent  component  of 
the  abdominal  venous  complex,  as  described  above  for  certain 
stages  in  the  development  of  the  cat  (pp.  29  to  33  and  figs.  20  to  24). 
Its  place,  however,  is  partially  occupied  by  an  early  lymphatic 
plexus  de\  eloped  in  the  preaortic  mesoderm  from  the  omphalo- 
mesenteric anlages  caudad.  Here  we  are  apparently  dealing  with 
an  instance  in  which  general  phylogenetic  venous  lines  have  been 
almost  or  entirely  abandoned  in  favor  of  other  pathways. 
Such  lines  appear,  however,  to  be  retained  under  these  con- 
ditions in  the  lymphatic  organization.  Thus,  the  spaces  just 
referred  to,  as  will  be  shown  subsequently,  form  the  first  incep- 
tion of  the  extensive  network  of  lymphatic  vessels  which  in  the 
adult  cat  surrounds  the  aorta  and  the  origin  of  the  superior 
mesenteric  artery,  closely  interwoven  with  the  semilunar  sym- 
pathetic and  the  adrenal  plexus,  and  connecting  on  the  one 
hand  with  the  portal  and  intestinal  lymphatics,  and  on  the  other 
with  the  beginning  of  the  thoracic  duct.  This  adult  mammalian 
lymphatic  plexus  forms  a  perfect  lymphatic  shadow-picture  of 
the  lacertilian  ontogenetic  peri-omphalomesenteric  venous  ring. 

In  conclusion,  I  wish  to  give  briefly  a  summary  of  my  reasons 
for  regarding  the  structures  described  in  this  communication  as 
the  anlages  of  the  systemic  lymphatic  vessels. 

"Except,  as  recently  determined,  in  Tragulus,  in  wnich  Ungulate  the  adult 
postcaval  system  is  of  the  marsupial  type,  and  in  certain  embryonic  stages  of  the 
Cat  (15. 5-17  mm.)  in  which  the  channels  appear  as  evanescent  preaortic  vessels, 
subsequently  entirely  replaced  by  lymphatics.  (Cf.  series  258;  figs.  20  to  24.) 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM          51 

These  early  lymphatic  anlages,  whether  formed  independently 
in  mesoderm,  or  on  the  site  of  phylogenetically  abandoned  venous 
lines,  or,  as  is  generally  the  case  throughout  the  body,  in  close 
correlation  to  the  embryonic  venous  pathways,  always  appear 
in  the  same  situations  and,  in  the  average  embryo,  at  the  same 
developmental  period.  Their  constant  character,  and  regular 
occurrence  and  relations,  repeated  within  very  narrow  limits  of 
individual  variation  in  every  embryo  of  the  proper  stage,  imparts 
to  them  a  definite  morphological  character.  In  every  series  of  the 
proper  age  in  my  collection  I  find  the  same  spaces  in  the  same 
place  and  in  identical  relationship  to  the  adjacent  veins.  In  some 
individuals,  as  above  stated,  they  develop  earlier  than  usual,  in 
others  their  appearance  is  retarded,  but  this  applies  only  to  the 
achievement  of  the  full  development  typical  for  the  average  embryo 
of  a  given  stage.  In  the  retarded  individuals  the  same  structures 
are  always  present,  only  they  are  less  strikingly  developed  and  less 
numerous  when  compared  with  the  average  normal  type  charac- 
teristic of  the  period  under  consideration.  With  sufficient  mag- 
nification it  is  not  difficult  to  distinguish  sharply  between  the 
perihaemal  lymphatic  spaces  and  the  blood-vascular  channels 
proper. 

With  sufficient  material  every  stage  of  their  development  can 
be  followed  up  to  the  confluence  of  the  entire  system  and  its  final 
entrance  into  the  jugular  lymph  sacs. 

These  spaces  are  neither  artefacts  due  to  embryonic  shrinkage, 
nor  are  they  the  unfilled  portions  of  the  blood-vascular  capillary 
network.  They  are,  on  the  other  hand,  the  well-defined  earliest 
anlages  of  the  systemic  lymphatic  vessels.  The  more  perfect,  as 
a  matter  of  fact,  the  embryonic  fixation  is,  the  more  clearly  can 
these  structures  be  ^identified  under  the  microscope.  Their 
history,  as  will  be  shown  presently,  can  be  traced  with  the  utmost 
accuracy,  and  they  can  be  followed  step  by  step  in  their  de- 
velopment up  to  their  inclusion  in  the  completed  and  connected 
lymphatic  channel  system. 

But  even  in  their  earliest  stages  they  possess  an  unmistakable 
and  definite  morphological  character,  quite  as  distinct  as  that 
of  the  adjacent  blood  channels.  They  can  be  followed  closely  in 


52         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

good  serial  sections  of  the  proper  thickness  and  fixation,  and  can 
be  reconstructed  in  the  same  manner  and  with  the  same  accuracy 
and  certainty  as  the  blood  channels  with  which  they  are  for  the 
most  part  so  closely  associated,  although  their  lumen  connects  at 
no  point  with  that  of  the  vascular  channels. 

These  statements  are  based,  not  on  isolated  observations,  but 
on  the  close  and  repeated  examination  of  a  very  large  number  of 
embryos  of  the  same  form.  It  seems  curious  to  me  that  the  pres- 
ence of  the  first  lymphatic  anlages,  as  above  described,  should  be 
denied,  or,  as  has  been  recently  done,  that  the  isolated  appear- 
ance of  these  spaces  should  be  ascribed  to  the  " sudden  collapsing" 
of  a  lymph  vessel.  At  the  time  at  which  they  make  their  first 
appearance  there  are  no  " lymph  vessels"  to  " collapse,"  no  more 
than  there  are  in  the  homologous  haemal  ontogenetic  stages  blood- 
vessels in  the  sense  of  continuous  channels.  On  the  contrary, 
when  they  reach  their  period  of  most  striking  development  (cat, 
13-14  mm.)  these  perivenous  lymphatic  spaces  are,  if  anything, 
distended,  not  only  by  their  fluid  contents,  but  by  the  remnant 
of  the  embryonic  atrophying  vein  which  they  are  in  the  process 
of  replacing.  The  only  structure  showing  any  sign  of  "collapse" 
is  the  empty  endothelial  bag  of  the  decadent  venule.  The  spaces 
become  relatively  reduced  in  size  in  the  later  stages,  after  the 
multiple  separate  early  anlages  have  fused  into  a  more  continu- 
ous lymphatic  channel  system. 

These  spaces  are  always  present  in  embryos  of  the  proper  stages 
in  the  typical  position  and  in  constant  relation  to  the  venous 
channels.  By  following  carefully  and  with  sufficient  material 
their  further  growth  and  development  in  succeeding  stages,  a  clear 
and  consecutive  picture  of  systemic  lymphatic  genesis  is  given. 

It  is  noteworthy,  in  view  of  the  incorrect  statements  published 
to  the  contrary,  that  these  primary  anlages  of  the  systemic  lym- 
phatic system  develop  constantly  in  embryos  of  the  cat  before  the 
definite  organization  of  the  jugular  lymph  sacs.  These  latter 
structures,  in  the  10  mm.  cat  embryo,  are  still  largely  in  the  con- 
dition of  a  perivenous  capillary  plexus,  at  a  time  when  the  first 
lymphatic  anlages  can  be  distinctly  recognized  in  the  axial 
mesoderm. 


RELATION  OF  LYMPHATIC  TO  BLOOD-VASCULAR  SYSTEM  53 

In  view  of  the  fact  that  these  first  anlages  can  be  traced  step 
by  step  as  developing  into  the  systemic  lympnatic  channels  of  the 
adult,  it  becomes  apparent  that  their  origin  cannot  be  ascribed 
to  " outgrowths"  from  the  jugular  sacs,  as  yet  not  formed.  A 
similar  lack  of  correct  reasoning  appears  in  portions  of  the  recent 
anatomical  literature  in  reference  to  the  injection  of  lymphatics 
in  the  early  stages.  It  is  manifestly  impossible  to  inject  some- 
thing which  does  not  as  yet  exist  in  the  form  of  a  continous  and 
injectable  system  of  communicating  channels.  The  spaces  which 
I  am  describing  and  which  I  regard  as  the  first  anlages  of  the 
systemic  lymphatics  cannot  be  injected  at  the  time  of  their  first 
appearance  because  they  are  intercellular  spaces,  extremely  nu- 
merous, but  as  yet  isolated  from  each  other,  and  not  in  communi- 
cation with  veins  or  with  anything  else  that  could  be  injected, 
in  the  sense  of  filling  a  lumen  artificially  with  a  colored  fluid,  or 
air,  or  any  other  foreign  substance.  They  multiply  rapidly, 
become  confluent  to  form  larger  spaces,  and  these  finally  unite 
into  continuous  channels.  But  the  genetic  determination  of  the 
origin  of  the  lymphatic  system  must  be  based  on  the  close  study 
of  embryonic  stages  long  prior  to  the  formation  of  continuous 
channels  capable  of  injection.  Where  lymphatic  vessels  can  once 
be  demonstrated  by  this  method  they  have  passed  the  formative 
stage.  It  then  becomes  merely  a  question  of  topographical  ex- 
tension and  readjustment,  such  as  is  encountered  in  all  vascular 
structures  alike  in  the  later  embryonic  periods. 

The  real  problem  of  the  genesis  of  the  lymphatics  can  only  be 
solved  by  the  recognition  of  tne  earliest  formative  stages,  begin- 
ning with  the  first  appearance  of  the  mesodermal  spaces  above 
described. 

Finally  I  can  sum  up  my  observations,  and  the  views  thereon 
based,  as  follows: 

1  The  systemic  lymphatic  vessels  of  the  entire  body  arise,  in 
the  mammalian  embryo,  by  confluence  of  mesodermal  spaces, 
developed  on  the  same  lines  as  those  governing  the  formation  of 
the  earliest  haemal  vascular  channels,  but  independent  of  the 
same. 


54         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

2  The  lymphatic  endothelium  is  an  independent  modifica- 
tion of  the  mesodermai  cells  lining  the  first  anlages  of  the  lym- 
phatic   spaces,    and  is  not  derived  from  the  haemal   vascular 
endothelium. 

3  I  am  obliged  to  deny  the  assumption  that  the  mammalian 
systemic  lymphatic  vessels  arise  by  the  confluence  of  numerous 
elements  detached  in  course  of  development  from  the  embryonic 
veins. 

4  I  am  obliged  to  put  myself  emphatically  on  record  against 
the  assumption  that  the  mammalian  systemic  lymphatic  vessels 
arise  by  a  progressive  sprouting  from  center  to  periphery  from 
the  endothelium  of  veins,  or  from  that  lining  the  jugular  lymph 
sacs,  or  equivalent  structures  in  other  regions  of  the  body.    The 
mammalian  embrvo  offers  no  evidence  of  such  occurrences. 


PART  I,  PLATES 

FIGURES  1  TO  28 

The  series  here  figured  and  described  are  in  the  embryological  collection  of 
Columbia  University,  with  the  exception  of  series  34,  which  belongs  to  the  em- 
bryological collection  of  Princeton  University.  I  am  greatly  indebted  to  Prof. 
C.  F.  W.  McClure  for  the  opportunity  of  studying  this  series  and  publishing  the 
eight  sections  shown  in  figs.  245  to  251. 


FIGURE  1 

1     Transverse  section  of  10  mm.  cat  embryo  (series  111,  slide  VIII,  section  4), 
X  175— Topographical  picture  of  site  of  earliest  lymphatic  space  development. 

1  Sympathetic  nerve. 

8  Oesophagus. 

68  Left  postcardinal  vein. 

69  Lungs. 

72  Right  dorsal  aorta. 

73  Left  dorsal  aorta. 

77  Mesenehymal  intercellular  lymphatic  anlages. 

78  Coelom. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  1 


MEMOIR  NO.    1,   HUNTINGTON,    1911 


FIGURE  2 

2     Transverse  section  of  10  mm.  cat  embryo  (series  111.  slide  VIII.  section  4) 
X  300— left  side  of  embryo. 

68  Left  post  cardinal  vein. 

73  Left  dorsal  aorta. 

77  Mesenchymal  intercellular  lymphatic  anlages. 

78  Coelom. 

79  Coelomic  stoma. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   2 


MEMOIR    NO.    1,    HUNTINOTON,    1911 


FIGURE  3 
3    Same.  X  600. 


THE   SYSTEMIC    LYMPHATIC   VESSELS 


PLATE   3 


MEMOIR  NO.    1,   HCJNTINGTON,   1911 


FIGURES  4  AND  5 

4  Transverse  section  of  10  mm.  cat  embryo  (series  111.  slide  VIII,  section  6), 
X  300. 

5  Same,  section  7. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  4 


MEMOIR  NO.   1,  HUNTINGTON,   1911 


FIGURES  6  AND  7 


6  Same,  section  8. 

7  Same,  section  9. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  o 


MEMOIR  NO.   1,  HCNTINGTON,   1911 


FIGURES  8  AND  9 

8  Transverse  section  of  10  mm.  cat  embryo  (series  120,  slide  IX,  section  25) 
X  300. 

9  Same,  section  26. 

1  Sympathetic  nerve. 

68  Left  postcardinal  vein. 

73  Left  dorsal  aorta. 

77  Mesenchymal  intercellular  lymphatic  anlages. 

78  Coelom. 


THE   .SYSTEMIC  LYMPHATIC  VESSELS 


PLATE    6 


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MEMOIR   NO.    1,   HCNT1NGTON,    1911 


FIGURES  10  AND  11 

10  Transverse  section  of  anterior  thoracic  region  of  12  mm.  cat  embryo  (series 
217,  slide  X,  section  12),  X  225— showing  early  extraintimal  lymphatic  develop- 
ment. 

11  Transverse  section  of  anterior  thoracic  region  in  a  12  mm.  cat  embryo  (series 
211,  slide  X,  section  15),  X  225. 

3  Precardinal  or  precava,  resp.  azygos  of  right  side. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 

6  Precardinal  or  precava,  resp.  azygos  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10     Pulmonary  artery. 
22    Vagus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE    7 


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MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURE  12 

12    Transverse  section  of  anterior  thoracic  region  in  a  14  mm.  embryo  (series 
127,  slide  VIII,  section  12),  X  225. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic    space    surrounding    degen- 

erating embryonal  vein. 

6  Precardinal  or  precava,  resp.  azygos  of  left  side. 
6'    Left  asygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE    8 


12 


MKMOIU    NO.    1,    HUNTINGTON,    1911 


FIGURES  13  AND  14 

0 

13  Transverse  section  of  anterior  thoracic  region  in  a  15  mm.  cat  embryo  (series 
219,  slide  XIV,  section  17),  X  225. 

14  Same,  section  18. 

6  Precardinal  or  precava,  resp.  azygos  of  left  side. 
6'  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

15  Interazygos  segment  of  thoracic  duct. 

22  Vagus. 

36  Azygos  segment  of  thoracic  duct. 

53  Precaval  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE    9 


15 


36 


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MEMOIR  NO.   1,   HUNTINOTON,   1911 


FIGURE  15 

15    Transverse  section  through  lower  cervical  region  of  a  14  mm.  cat  embryo 
(series  222,  slide  VII,  section  26),  X  150. 

11  Jugular  lymph  sac. 

25  Internal  jugular  vein. 

27  External  jugular  vein. 

27'  External  jugular  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  10 


15 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURE  16 
Hi    Same,  slide  VIII,  section  4. 

11  Jugular  lymph  sac. 

25  Internal  jugular  vein. 

27  External  jugular  vein. 

27'  External  jugular  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  11 


11 


MEMOIR   NO.   1,    HUNTINGTON,   1911 


FIGURE  17 

17     Transverse  section  of  upper  thoracic  region  of  14  mm.  embryo  (series  37, 
slide  XIII,  section  12),  X  150. 

1  Sympathetic  nerve. 

3  Precardinal  or  precava,  resp.  azygos  of  right  side. 

6  Precardinal  or  precava,  resp.  a^ygos  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 
22  Vagus. 

53     Precaval  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  12 


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•MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  18  AXD  19 

18  Transverse  section  of  middle  thoracic  region  in  a  17  mm.  cat  embryo  (series 
258,  slide  XVIII,  section  9),  X  225. 

19  Transverse  section  through  mid-thoracic  region  of  a  19  mm.  cat  embryo 
(series  253,  slide  XXIV,  section  9),  X  225. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos. 

4  Atrophying  embryonal  vein. 

5  Extraintimal  or  perivenous  lymphatic  space. 

6  Left  azygos. 

7  Aorta. 

15     Interazygos  venous  plexus. 

36    Azygos  segment  of  thoracic  duct. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 
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MEMOIR   NO.    1,   HUXTIXGTOX,    1911 


FIGURE  20 

20  Transverse  section  of  upper  abdominal  region  of  a  17  mm.  cat  embryo,  show- 
ing developing  components  of  ascending  lumbar  lymphatic  trunks  and  of  mesen- 
teric  sac  in  relation  to  embryonic  veins  in  the  root  of  the  dorsal  mesentery  and  their 
relation  to  the  cardinal  collateral  venous  channels  (series  258,  slide  XXIII,  section 
34),  X  75. 

1  Sympathetic  nerve. 

7  Aorta. 

51  Mesenteric  lymphatics. 

58  Ureters. 

61  Iliac  vessels. 

62  End  gut. 

63  Ventral  division  of  cloaca  (urinary  bladder). 

64  Wolffian  ducts. 

66  Umbilical  arteries. 

67  Right  postcardinal  vein. 

68  Left  postcardinal  vein. 

74  Cardinal  collateral  veins. 

75  .Ascending  lumbar  lymphatic  trunks. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  14 


'..jteW^j^i,. 
•r  •:<*»>•,  -.      ' 


67 


if*;  m^Wi^ 

wjmi^jl?  i^lptspift    '%i^$^ 


.SA 


75 


51 


68 


••-  -'%V-%T  j2>V*  •*"*'•  -"i-  r-I>;  .--'Tr^---T  '• ***  •"<• -11  —  -11  y  ..'•••'  ^  >  *'  •'  /wtinr'ivvy.-. 

raHf4f  mX.  t  9n '  'ft  •       •'»<'«  u'*  J  ttfiBfcJi  *.  t  «,/rirfla  mil  ;ifci  •«,_  .%_••  ff  •  ,/^_  ,  ».»*  y,.»  *  x ' MkK  u— r »  !' .  !*~aSHS 


75 


74 


61 


T£\:^';^^\^fe^ML^^ 


Jafe  vJ-  'i1'.'-*.'!-1?'11:  ^AM^T-r^V^ 


20 


MEMOIR   NO.   1,   HUNTINGTON,    1911 


FIGURE  21 
21     Same  section,  X  150. 

7  Aorta. 

51  Mesenteric  lymphatics. 

58  Ureters. 

67  Right  postcardinal  vein. 

68  Left  postcardinal  vein. 

74  Cardinal  collateral  veins. 

75  Ascending  lumbar  lymphatic  trunks. 


THE   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE   15 


21 


Ml..\  (Hi    NO.   ].  HfNTTNCTf.N,  1011 


FIGURE  22 
22    Same,  section  33. 

1  Sympathetic  nerve. 

7  Aorta. 

51  Mesenteric  lymphatics. 

58  Ureters. 

67  Right  postcardinal  vein. 

68  Left  postcardinal  vein. 

74  Cardinal  collateral  veins. 

75  Ascending  lumbar  lymphatic  trunks. 


THE   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE  16 


22 


MBMOITt  NO.  1,  HtTXTINGTON,  1011 


FICURKS  23  AND  24 


23  Same,  section  32. 

24  Same,  section  31. 

7  Aorta. 

51  Mesenteric  lymphatics. 

67  Right  postcardinal  vein. 

68  Left  postcardinal  vein. 

74  Cardinal  collateral  veins. 

75  Ascending  lumbar  lymphatic  trunks. 


I  111';   SYSTKMIC    LYMPHATIC   VKSSKLS 


PLATE  17 


67 


23 


MEMOIR   NO.   1,   HUNTIXGTON,   1911 


FIGURE  25 

25  Transverse  section  of  posterior  end  of  a  20  mm.  cat  embryo  (series  241, 
slide  XXX,  section  4),  X  75 — showing  cxtraintimal  replacement  of  left  supra  car- 
dinal vein  (59)  by  ascending  lumbar  retroaortic  lymphatic  channel  (76). 

1  Sympathetic  nerve. 

7  Aorta. 

58  Ureters. 

59  Left  supracardinal  vein. 

60  Right  supracardinal  vein. 

62  End  gut. 

63  Ventral  division  of  cloaca  (urinary  bladder). 

64  Wolffian  ducts. 

65  Metanephros. 

66  Umbilical  arteries. 

67  Right  postcardinal  vein. 

68  Left  postcardinal  vein. 

76     Retroaortic  supracardinal  lymphatic  trunks. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  18 


M-GMOIR   NO.    1,    HUNTINGTON,    1911 


25 


FIGURE  26 
26    Same,  section  14,  X  150. 

1  Sympathetic  nerve. 

58  Ureters . . 

59  Left  supracardinal  vein. 

60  Right  supracardinal  vein. 

67  Right  postcardinal  vein. 

68  Left  postcardinal  vein. 

75  Ascending  lumbar  lymphatic  trunks. 

76  Retroaortic  supracardinal  lymphatic  trunks. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   19 


75 


26 


MEMOIR   NO.   1,    HUNTINGTON,    1911 


FIGURE  27 

27     Reconstruction  of  anterior  vascular  complex  in  an   18  mm.  cat  embryo 
(series  88),  X  50.     Ventral  view. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  20 


LEFT    INT.  JUG.   V. 


EXT.  JUG.  V 


JUGULAR   APPROACH 
THYRO  CERVICAL   A. 
LEFT   COMMON    JUGULAR    VEIN 


EFT   SUBCLAVIAN 


LEFT    SUBCLAVIAN    V. 


INT.  MAMMARY  A. 


PRECAVALELYMPHATIC 


INNOMINATE   A. 


RIGHT  PRECAVA 


LEFT   PRECAVA 


27 


MBMOIIt    NO.    1,   HUNTING-TON,    1911 


FIGURE  28 
28    Same,  lateral  view  of  left  side. 


THE  SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  21 


LEFT    INT.   JUG.   V 


LEFT    EXT.  JUG.  V. 


JUGULAR   APPROACH 


THYRO-CERVICAL  A. 


LEFT   COMMON   JUGULAR   VEIN 


LEFT   SUBCLAVIAN    V. 


LEFT   SUBCLAVIAN    A 


INT.  MAMMARY    A    ANDV. 


RIGHT  PRECAVA 


INNOMINATE   A 


LEFT   CEPHALIC  VEIN 


LEFT 
SUBCLAVIAN  APPROACH 


JUGULO-SUBCLAVIAN  TAP 
THYRO-CERVICAL  A. 


—  SUBCLAVIAN  A 
THORACIC  DUCT 

LEFT   PRECAVA 


28 


MEMOIR   NO.    1,   HUNTINOTON,    1911 


PART  II 

THE  DEVELOPMENT  OF  THE  PREAZYGOS  AND  AZY- 
GOS  SEGMENTS  OF  THE  THORACIC  DUCTS 

In  certain  developmental  stages  in  the  cat,  the  embryonic 
anlages  of  the  thoracic  ducts  appear  as  potentially  symmetrical 
bilateral  lymphatic  channels. 

Subsequently,  the  cephalic  portion  of  the  left  duct,  having 
secondarily  assumed  the  function  of  conveying  the  lymph  from 
the  trunk  and  the  posterior  extremities,  forms,  cephalad  to  the 
aortic  arch  level,  the  main  continuation  of  the  thoracic  duct 
proper,  emptying,  through  the  intervention  of  the  left  jugular 
lymph  sac,  into  the  general  venous  system  at  the  left  common 
jugular  confluence,  or  at  the  jugulo-subclavian  junction,  or  at 
both  of  these  points,  according  to  the  type  of  adult  lymphatico- 
venous  connection  established  in  individual  cases  (26)>  (2?;>  (34)> (35;> 

The  corresponding  cephalic  preazygos  portion  of  the  right  lym- 
phatic duct  then  remains  as  a  more  or  less  rudimentary  structure, 
draining  the  anterior  mediastinal  region  and  emptying  into  the 
right  jugular  lymph  sac. 

Caudad  of  the  level  of  the  aortic  arch,  the  adult  thoracic  duct 
is  a  composite  of  parts  of  three  embryonic  lymph  channels  pre- 
senting a  great  range  of  individual  variation.  Two  of  these 
anlages  develop  as  bilateral  extraintimal  lymphatic  trunks  along 
the  ventral  aspect  of  the  right  and  left  azygos  veins.  The  third 
intermediate  channel,  which  is  the  first  to  distinctly  differentiate 
in  the  embryo  and  is  the  main  element  in  the  typical  organiza- 
tion of  the  adult  duct,  develops  in  the  caudal  portion  from  ex- 
traintimal lymphatic  anlages,  which  replace  part  of  the  ventro- 
medial  tributary  plexus  of  the  right  azygos  vein.  In  ascending 

35  C.  F.  W.  McClure  and  C.  F.  Silvester:  "A  comparative  study  of  the  Lym- 
phatic-Venous communications  in  Adult  Mammals,"  Anat.  Rec.,  Vol.  Ill,  pp. 
634-551. 

55 


56       DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

it  increasingly  turns  to  the  left  and  continues  to  develop  cephalad 
along  the  ventral  surface  of  the  inter-azygos  plexus,  by  extra- 
intimal  replacement  of  elements  belonging  to  the  latter.  (Com- 
pare the  series  of  six  reconstructions  shown  in  figs.  188,  189, 
190,  191,  192,  193.) 

The  details  of  the  adult  organization  of  the  thoracic  ducts,  and 
the  genesis  of  the  observed  adult  variations  on  the  basis  of  the 
development  of  the  embryonic  channels,  will  be  considered  subse- 
quently (Part  V).  The  present  communication  is  confined  to 
the  consideration  of  the  development  of  the  preazygos  and 
azygos  segments  of  the  ducts.  The  thoracic  ducts  develop  in  cat 
embryos  between  11  and  16  mni.  crown  rump  measure.  In  the 
16  mm.  embryo,  McClure  (15J  states  that  they  "for  the  first 
time  make  their  appearance  as  definite,  continuous  lymph  chan- 
nels, which  are  disconnected  from  the  venous  system,  except 
through  the  mediation  of  the  jugular  lymph  sacs."  This  is  the 
case  in  the  majority  of  16  mm.  embryos,  but  in  a  number  of  15, 
15.5  and  16  mm.  series  in  my  collection  the  final  union  of  the 
individual  segments  has  not  yet  taken  place.  It  is  possible,  by 
combining  a  large  number  of  observations  on  numerous  embryos 
of  the  same  length,  to  establish  an  average  developmental  condi- 
tion of  the  thoracic  ducts  for  each  stage  in  embryos  between  12 
mm.  and  17  mm.  crown-rump  measure.  Individual  embryos 
will,  however,  show  marked  differences  in  development,  and 
many  departures  from  the  standard  plan  are  encountered. 
The  same  conditions  obtain  here  which  McClure  and  I  found  in 
our  study  of  the  development  of  the  jugular  lymph  sacs.  Some 
embryos  show,  for  their  length,  unusually  advanced  thoracic 
duct  development  in  certain  areas,  while  in  other  parts  this 
development  is  relatively  retarded  and  more  primitive.  In  other 
series  the  entire  region  of  thoracic  duct  development  appears 
more  uniformly  ahead  of  the  average  condition,  normally  en- 
countered in  embryos  of  this  period.  Finally,  in  a  third  group, 
the  appearance  of  the  typical  lymphatic  development  seems  to 
be  delayed  until  a  later  stage  than  is  normally  the  case.  But  in 
spite  of  these  individual  differences,  a  uniform  and  consistent 
ground  plan  of  thoracic  duct  development  can  be  demonstrated,  to 


DEVELOPMENT  OF  THE  THORACIC  DUCT          57 

which  the  majority  of  embryos  conform  and  into  which  even  the 
aberrant  types  fit.  As  a  matter  of  fact,  the  regularity  with  which 
the  thoracic  duct  anlages  first  appear  in  the  majority  of  the 
individuals  of  the  proper  stage,  and  the  uniform  and  constant 
character  of  the  resulting  histological  pictures,  is  one  of  the  most 
striking  and  significant  features  of  the  entire  process.  Prior  to 
the  11  mm.  stage  no  definite  anlage  of  the  anterior  segments  of 
the  future  ducts  is  observable.  . 

I  believe  that  the  adult  thoracic  ducts  of  the  cat  are  developed 
by  fusion  of  three  distinct  and  separate  regional  segments.  Each 
of  these  segments  is  in  turn  formed  by  confluence  of  a  number  of 
originally  discrete  and  independent  anlages,  which  develop  inde- 
pendently of  the  venous  system  as  extra-intimal  or  perivenous 
mesenchymal  spaces  in  the  sense  previously  defined.  (1»  2>  21> 
22)-  These  spaces  are  applied  to,  or  surround,  the  walls  of 
the  embryonic  veins  of  the  lower  cervical  and  of  the  dorsal 
mediastinal  region.  The  three  main  divisions,  thus  developed 
independently  of  the  venous  system,  unite  with  each  other  to 
form  the  channels  of  the  left  and  right  thoracic  ducts,  and  these 
usually  gain  their  point  of  entrance  into  the  systemic  veins  by 
uniting  with  a  process  of  the  jugular  lymph  sacs  ("  thoracic  duct 
approach")  derived  from  their  dorsal  aspect,  just  cephalad  to 
the  common  jugular  approach.  Exceptionally  the  main  (left) 
thoracic  duct,  by  combining  with  the  ventral  mediastinal  trunk 
presently  to  be  described,  unites  (fig.  98)  with  the  ventral  process 
of  the  "subclavian  approach,"  prolonged  from  the  jugular  lymph 
sac  over  the  ventral  surface  of  the  jugulo-subclavian  confluence, 
and  thus  establishes  its  connection  with  the  venous  system  (cf. 
pp.  84  89,  figs.  89  to  99). 

The  ontogenetic  history  of  the  ducts  may  therefore  (fig.  29) 
be  considered  under  four  headings,  viz.: 

1.  THE  THORACIC  DUCT  APPROACH  of  the  jugular  lymph  sac, 
forming  the  terminal  of  the  adult  duct  on  each  side  (fig.  29, 1,  blue). 

2.  THE  PREAZYGOS  SEGMENT  (fig.  29,  II).    This  includes  two 
distinct  and  separate  channels: 

A.  The  broncho-mediastinal  or  ventral  mediastinal  lymphatic 
trunk  (fig.  29,  37.  green),  which  drains  the  ventral  mediastinum 


58         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

cephalad  of  the  pericardium,  viz.,  the  pericardial,  tracheal, 
bronchial,  lateral  oesophageal,  and  thymic  areas. 

This  lymphatic  channel,  associated  with  the  embryonic  venous 
plexuses  of  the  pretracheal  region,  the  pulmonary  vessels  and 
the  vagi,  develops  through  confluence  of  a  large  number  of  sep- 
arate and  independent  extra-intimal  lymphatic  spaces  following 
and  surrounding  the  embryonic  venous  plexuses  of  the  ventral 
mediastinum.  The  chain  formed  by  these  spaces  eventually 
unites  with  the  similar  chain  forming  the  anlages  of  the  preazygos 
segment  of  the  thoracic  duct. 

B.  The  preazygos  segment  of  the  main  thoracic  duct  (fig.  29,  35, 
brown).  This  portion  of  the  main  duct  extends  from  the  point 
of  its  entrance  into  the  jugular  lymph  sac,  through  the  thoracic 
duct  approach  of  the  latter,  caudad  to  its  intersection  with  the 
dorsal  surface  of  the  aortic  arch. 

In  the  adult  animal  this  segment  forms  the  relatively  long  por- 
tion which  ascends  cephalo-sinistrad  from  the  point  where  the 
duct  parts  company  with  the  right  azygos  vein,  to  its  junction 
with  the  jugular  lymph  sac,  under  cover  of  the  aortic  arch,  and 
the  vertical  portion  of  the  left  subclavian  artery,  dorsal  to  the 
vertebral  vein  and  to  the  left  innominate  confluence.  In  this 
part  of  its  course  the  thoracic  duct  frequently  receives  the  lym- 
phatic return  from  the  ventral  mediastinum  through  channels 
which  unite  it  to  the  ventral  mediastinal  trunk  as  just  defined. 
The  preazygos  segment  of  the  main  duct  is  again  formed  in  the 
embryo  by  confluence  of  independent  mesenchymal  spaces 
around  and  along  the  prevertebral  and  dorsal  mediastinal  venous 
plexuses  of  the  embryo. 

3.  THE  AZYGOS  SEGMENT  (fig.  29,  III,  36,  yellow)  comprises 
the  portions  of  the  thoracic  ducts  caudal  to  the  level  of  the  aortic 
arch.     It  develops,  again  independently,  as  the  result  of  fusion 
of  a  number  of  extraintimal  mesenchymal  spaces  closely  applied 
to  the  ventral  surface  of  the  azygos  veins,  or  of  their  ventro- 
medial  tributaries,  or  surrounding  the  latter. 

4.  THE  POST- AZYGOS  SEGMENT  (fig.  29,  IV,  52,  green),  through 
which  the  thoracic  ducts  establish  their  connection  with  the 
Receptaculum  and  the  system  of  the  abdominal  lymphatics. 


DEVELOPMENT  OF  THE  THORACIC  DUCT  59 

Inasmuch  as  the  development  of  this  segment  of  both  ducts 
is  intimately  connected  with  that  of  the  principal  abdominal 
lymphatic  channels,  its  consideration  will  be  included  in  that  of 
the  latter  system  (Part  III).  The  present  communication  deals 
only  with  the  first  three  segments  above  enumerated. 

Fig.  29  shows  in  a  color  schema  the  genetic  composition  of  the 
thoracic  ducts  according  to  the  segments  just  outlined,  and  their 
relation  to  the  embryonic  venous  system.  . 

In  proceeding  caudo-cephalad  the  post-azygos  portion  (IV) 
develops  in  the  larger  right  segment  (52)  by  replacement  of  the 
caudal  part  of  the  ventro-medial  tributary  plexus  of  the  right 
azygos  vein. 

The  smaller  channel  of  the  left  side  replaces  the  caudal  part  of 
the  left  azygos  vein.  In  the  azygos  area  (III)  the  left  channel 
follows,  as  a  much  reduced  left  thoracic  duct,  the  prevertebral 
portion  of  the  left  azygos  vein.  The  larger  right  lymphatic 
channel  (36),  gradually  inclining  cephalo-sinistrad,  develops 
along  the  ventral  aspect  of  the  inter-azygos  cross-anastomosis 
and  unites  with  the  left  duct  eventually  in  a  close  plexiform  inter- 
lacement perforated  by  the  intersegmental  arteries,  which  con- 
tinues cephalad  to  near  the  level  of  the  aortic  arch.  Here  the 
plexus  condenses  into  two  more  or  less  well  defined  channels 
which  turn  up  to  the  right  and  left  into  the  preazygos  segment 
(II).  The  smaller  right  channel  follows,  cephalad  of  the  right 
azygos  terminal,  the  dorso-medial  aspect  of  the  right  precaval, 
innominate  and  common  jugular  veins,  developing  by  confluence 
of  extraintimal  spaces  along  the  course  of  these  vessels  (cf .  recon- 
struction of  series  88,  figs.  27  and  28),  and  forms  the  cephalic 
end  of  the  reduced  right  thoracic  duct  of  the  adult.  It  terminates 
by  joining  the  thoracic  duct  approach  (12)  of  the  right  jugular 
lymph  sac.  The  left  and  larger  trunk  replaces  the  extra-peri- 
cardial  portion  of  the  left  precava,  and  ascends  dorsal  to  the  left 
innominate  confluence  to  its  junction  with  the  thoracic  duct 
approach  (12)  of  the  left  jugular  lymph  sac.  37  in  fig.  29  indi- 
cates the  broncho-mediastinal  trunk  in  one  of  its  commonly 
encountered  types,  joining  caudally  the  preazygos  portion  of  the 
thoracic  duct  (35),  and  terminating  cephalad  in  the  ventral 


60        DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC    VESSELS 

process  of  the  subclavian  approach  (14)  of  the  jugular  lymph  sac, 
in  company  with  the  main  lymphatic  channels  returning  from 
the  anterior  extremity. 

1.     THE  THORACIC  DUCT  APPROACH  OF  THE  JUGULAR  LYMPH  SACS 

(FIG.   29,  18) 

This  structure  is  an  integral  part  of  the  jugular  lymph  sacs 
and  forms  in  the  adult  animal  the  portal  of  entry  of  the  thoracic 
ducts  into  the  lymph  sacs,  and  through  them  into  the  systemic 
veins.  McClure,  in  the  paper  quoted  Cl5)>  has  described  its 
general  formation  and  relation  to  the  jugular  lymph  sac  and  has 
given  an  excellent  illustration  of  its  appearance  in  the  dorsal 
view  of  a  reconstruction  of  a  14  mm.  cat  embryo.  I  have  here 
defined  it  as  the  "thoracic  duct  approach"  of  the  sacs,  in  con- 
formity with  the  nomenclature  which  McClure  and  I  adopted 
in  describing  (26>  27»)  the  development  of  those  portions  of  the 
jugular  sac  which,  forming  the  "  jugular"  and  "  subclavian" 
"approaches,"  project  as  blind  processes  from  the  caudal  end  of 
the  sac,  and  are  destined  to  effect  subsequently  the  permanent 
lymphatico-venous  connections  at  either  the  common  jugular, 
or  the  jugulo-subclavian  confluence,  or  at  both  of  these  venous  an- 
gles. The  term,  as  here  used  in  describing  the  similar  process  of 
the  sac  which  is  to  establish  definite  connections  with  the  thor- 
acic duct,  is  intended  to  emphasize  the  fact  that  the  '  'thoracic 
approach"  of  the  lymph  sac  is,  like  the  rest  of  the  structure  from 
which  it  proceeds,  venous  in  origin,  while  the  thoracic  ducts  proper, 
with  which  it  secondarily  unites,  are  not  derived  from  the  veins, 
but  are,  from  their  beginning,  independent  of  the  blood-vascular 
channels,  and  develop  by  confluence  of  independent  extra-  or  peri- 
venous  mesenchymal  spaces. 

This  fundamental  difference  in  origin  is  shared,  in  my  opinion, 
by  all  the  other  main  systemic  lymphatics  which,  in  addition  to 
the  thoracic  ducts,  enter  the  jugular  sacs  as  the  subclavian,  ex- 
ternal jugular,  cephalic  and  internal  jugular  lymphatics  through 
the  processes  which  the  sac  sends  to  meet  them. 

The  thoracic  duct  approach  of  the  earlier  embryos  arises  as  a 
short,  blunt,  curved,  conical  process  from  the  dorso-medial  aspect 


DEVELOPMENT  OF  THE  THORACIC  DUCT          61 

of  the  sac,  a  short  distance  cephalad  of  the  jugular  approach  and 
of  the  common  jugular  venous  confluence. 

It  extends  meso-caudad  across  the  dorso-lateral  and  dorsal 
aspects  of  the  internal  and  common  jugular  veins  between  them 
and  the  thyro-cervical  artery,  towards  the  vagus-sympathetic 
strand,  dipping  ventro-mesad  between  the  main  vein  and  the 
nerves  and  ending  blindly  in  this  situation. 

The  process  makes  its  first  distinct  appearance,  after  the 
jugular  sac  has  been  fully  established,  in  embryos  of  between  11 
mm.  and  14  mm.  crown-rump  measure. 

It  is  noteworthy  that  individual  embryos  within  these  limits 
show  considerable  difference  in  the  degree  of  development  of  the 
process.  In  some  it  appears  earlier,  in  others  a  little  later,  so 
that  in  individual  instances  an  embryo  of  slightly  shorter  measure 
may  have  the  thoracic  duct  approach  of  the  jugular  lymph  sac 
further  developed  than  one  which  exceeds  the  first  in  total  length 
by  the  fraction  of  a  millimeter. 

Thus  one  of  the  earliest  distinct  stages  of  the  process  is  seen 
in  a  14  mm.  embryo  (series  210,  slide  viii,  sections  39-42,  figs. 

30  to  33  inclusive). 

In  this  embryo,  the  thoracic  duct  approach  appears  as  a  short 
blunt  process  which  projects  dorso-mesad  from  the  caudal  end 
of  the  left  jugular  lymph  sac,  a  short  distance  cephalad  of  the 
common  jugular  confluence.  Sections  39,  40  and  41  (figs.  30, 

31  and  32,  12)  show  the  earliest  stage  in  the  development  of  this 
process.     In  them  the  area  dorsal  to  the  main  vein,  between  the 
sympathetic  nerve  and  the  jugular  lymph  sac,  is  occupied,  in 
the  direction  meso-laterad,  by  the  sympathetic  nerve    (1),  the 
termination   of    the   large   dorso-medial   venous  tributary  (left 
sup.  intercostal  vein)   (16),  the  thyro-cervical  artery  (24),.  and, 
laterad  to  this,  by  the  blind  terminal  portion  of   the  thoracic 
duct  approach  (12),  derived  from  the  dorso-medial  aspect  of  the 
jugular  lymph  sac  (11).     In  this  embryo  the  process  of  the  sac 
ends  blindly  laterad  to  the  thyro-cervical  artery  (figs.  33,  34,  24). 
It  has  not  yet  extended  meso-caudad  across  the  dorsal  surface  of 
the  main  vein  toward  the  interval  between  the  thyro-cervical 
artery  and  the  sympathetic  nerve.     The  thyro-cervical  artery 


62         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

(24)  lies  at  a  little  distance  directly  dorsad  of  the  internal  jugular 
vein.  The  dorso-medial  angle  of  the  main  vein  is  related  to  a 
large  compound  medial  venous  tributary,  draining  the  dorso- 
medial  (pre vertebral),  (17)  and  the  dorsal  somatic  areas  (16). 
This  compound  vessel  is  the  anlage  of  the  future  superior  inter- 
costal vein.  In  fig.  33  (section  42)  the  common  trunk  opens 
into  the  main  vein  just  dorsal  to  the  sympathetic  nerve  (/). 
In  this  section,  the  blunt  medial  extremity  of  the  thoracic  duct 
approach  (12)  is  separated  from  the  portion  still  connected  with 
the  jugular  lymph  sac,  thus  expressing  the  caudo-mesal  curve 
of  the  entire  process.  It  ends  blindly  in  the  following  section,  and 
does  not  reappear  in  the  succeeding  sections.  The  common  jugu- 
lar confluence  occurs  in  section  44  of  this  slide. 

We  are  dealing,  therefore,  with  a  short,  blunt  conical  process 
of  the  left  jugular  lymph  sac,  which  curves  meso-caudad  for  two 
sections,  and  terminates  blindly  dorsal  to  the  main  vein. 

In  another  14  mm.  embryo  (series  212)  the  thoracic  duct  ap- 
proach is  much  more  extensively  developed  and  occupies  sections 
11  to  26  of  slide  ix.  Selected  sections  of  this  series  are  shown 
in  figs.  34  to  42  inclusive. 

Fig.  34  (series  212,  slide  ix,  sec.  14)  shows  part  of  the  caudal 
end  of  the  left  jugular  lymph  sac  (11)  with  the  thoracic  duct 
approach  (12)  arising  from  its  medial  aspect  and  extending  mesad 
across  the  dorsal  surface  of  the  internal  jugular  vein  (25).  On 
the  mesal  aspect  of  the  vein  are  seen  the  sympathetic  (1)  and 
the  vagus  (22). 

The  large  common  trunk  formed  by  the  union  of  the  dorsal 
somatic  and  pre vertebral  venous  tributaries  (16,  17)  lies  dorso- 
medial  to  the  main  jugular  channel.  It  joins  the  latter,  as  left- 
superior  intercostal  vein,  (16,  4-6,)  in  section  26  of  this  slide 
(fig.  41).  On  the  lateral  aspect  of  this  vessel  is  the  ascending 
dorsal  branch  of  the  thyro-cervical  artery  (24). 

The  six  succeeding  figures  (35  to  40  inclusive)  are  cut  down  so 
as  to  only  show  the  dorsal  circumference  of  the  internal  jugular 
vein  and  the  superincumbent  thoracic  duct  approach  of  the 
jugular  lymph  sac. 

In  fig.  35  (section  15)  the  approach  has  extended  further  mesad 


DEVELOPMENT  OF  THE  THORACIC  DUCT  63 

across  the  main  vein.  In  fig.  36  (section  16)  a  blind  terminal 
protrusion  (12}  separates  from  the  main  lumen  of  the  sac  (11}, 
indicating  the  frequent  bifid  character  of  the  thoracic  duct  ap- 
proach. The  succeeding  sections  (18  and  20,  figs.  37  and  38) 
hence  show  an  apparent  recession  of  the  entire  process.  In  sec- 
tion 22  (fig.  39)  the  approach  has  again  extended  mesad  toward 
the  thyro-cervical  artery  and  the  superior  intercostal  vein.  In 
the  succeeding  section  (fig.  40)  the  fundus  of  the  process  terminates 
for  the  second  time  in  a  blind  pouch-like  protrusion  (12}.  In  the 
following  section  (24,  fig.  41)  the  approach  (12}  again  appears 
fully  developed  and  in  open  connection  with  the  main  jugular 
lymph  sac  (11}.  It  maintains  the  character  in  section  25,  and 
in  section  26  (fig.  42)  the  terminal  of  this  second  protrusion  (12} 
ends  blindly.  It  does  not  reappear  in  the  succeeding  sections. 

We  are  dealing  here  with  an  instance  of  very  common  occur- 
rence, in  which  the  thoracic  duct  approach  of  these  earlier  stages 
not  only  gives  off  a  number  of  blind  terminal  diverticula,  but  in 
which  the  entire  approach  arises  by  two  or  three  distinct  and 
separate  origins  from  the  main  jugular  lymph  sac.  This  character 
will  again  be  discussed  below  (cf.  p.  66).  in  connection  with  the 
interpretation  of  certain  adult  conditions,  but  the  instance  now 
under  discussion  shows  the  early  type  of  this  variation  very  clearly, 
so  that  in  a  graphic  reconstruction  the  thoracic  duct  approach 
of  this  embryo  would  appear  as  in  figure  on  page  64. 

This  embryo  therefore  presents  for  its  age  an  unusually  long 
and  well  developed  thoracic  duct  approach,  with  triple  terminal 
pouches,  extending  through  sixteen  sections,  while  at  the  same 
time  it  remains  throughout  this  extensive  course  in  the  early 
position,  viz.:  lateral  to  the  thyro-cervical  artery  (24)  and  the 
common  trunk  of  the  dorsal  and  dorso-medial  tributaries  of  the 
internal  jugular  vein  (16,  17,  46)-  The  approach  has  not  as  yet 
arched  mesad  into  the  neuro-venous  recess,  and  is  hence  in 
marked  contrast  to  the  succeeding  stages  presently  to  be  described. 

In  a  13.5  mm.  embryo,  series  189,  the  development  of  the  tho- 
racic duct  approach  has  gone  much  further,  although  the  embryo, 
a  litter  mate  of  series  210,  measures  half  a  millimeter  less. 

The  thoracic  duct  approach  of  the  left  jugular  lymph  sac 


64 


DEVELOPMENT    OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 


occupies  sections  10  to  23  of  slide  vii  in  this  embryo,  and  is 
shown  in  the  dorsal  view  of  the  reconstruction,  fig.  89,  to  which 
the  individual  sections  following  are  referred  for  orientation. 

The  process  arises  in  the  usual  situation  from  the  dorso-medial 
aspect  of  the  left  jugular  lymph  sac  and  trends  dorso-mesad 


f          12 

Sec.    16                Fit  36               /           >n 

/ 

Sec.   18-20  22    Fig.  37  38-39  \^S  / 

k                                                  7 

Sec    23              FiJ.  40                        I  SJ 

/ 

across  the  internal  jugular  vein  (series  189,  slide  vii,  section  10, 
fig.  43).  In  reference  to  the  level  of  the  common  jugular  conflu- 
ence, which  occurs  in  slide  vii,  section  26,  the  thoracic  duct 
approach  in  series  189  arises  more  anteriorly  from  the  jugular 
lymph  sac  than  in  the  preceding  series  210.  Its  extent  and  course 


DEVELOPMENT  OF  THE  THORACIC  DUCT  65 

can  be  followed  accurately  in  the  successive  sections  shown  in  figs. 
43  to  55  inclusive  (series  189,  slide  vii,  sections  10  to  22  inclusive). 

In  section  11  (fig.  44)  the  thoracic  duct  approach  is  separated 
by  a  thin  endothelial  partition  from  the  lumen  of  the  main  jugular 
lymph  sac,  which  it  rejoins  in  the  following  section  (section  12, 
fig.  45),  only  to  again  separate  in  the  next  section  (section  13, 
fig.  46).  In  the  meanwhile,  the  thoracic  duct  approach  has 
arched  from  the  lateral  to  the  medial  side  of  the  internal  jugular 
vein  (25),  closely  applied  to  its  dorsal  surface,  between  the  same 
and  the  thyro-cervical  artery  (24),  and  its  blind  terminal  is 
beginning  to  bend  ventro-mesad  into  the  neuro-venous  recess 
between  the  vagus-sympathetic  strand  (1,  22)  and  the  internal 
jugular  vein  (25).  In  the  next  three  sections  (sections  14,  15, 
16,  figs.  47,  48  and  49)  the  thoracic  duct  approach  becomes 
slightly  dilated  and  diverticular  (sections  15  and  16,  figs.  48  and 
49),  but  remains  detached  from  the  jugular  sac.  In  section  15 
(fig.  48)  it  appears  subdivided,  by  endothelial  partition,  into  two, 
and  in  section  16  (fig.  49)  into  three  components.  The  protru- 
sion which  the  common  jugular  confluence  sends  towards  the 
jugular  approach  of  the  lymph  sac  and  which  forms  the  point 
of  the  subsequent  invagination  of  the  venous  angle  by  the  lym- 
phatic tap,  begins  to  appear  in  section  16  (fig.  49),  and  can  be 
traced  through  the  succeeding  sections  as  a  derivative  of  the  lateral 
aspect  of  the  main  internal  jugular  vein,  between  it  and  the 
median  surface  of  the  jugular  lymphatic  sac. 

In  the  six  following  sections,  17  to  22  inclusive,  (figs.  50  to 
55  inclusive)  the  proximal  end  of  the  process,  connected  with  the 
sac,  gradually  recedes,  while  the  blind  distal  end  (12')  continues 
to  develop  in  the  ventro-medial  direction  between  the  main  vein 
(25,  in  fig.  55)  and  the  dorsal  and  dorso-medial  venous  tributaries 
(16  and  17,  fig.  55),  dipping  ventrad  and  approaching  the  interval 
between  the  internal  jugular  vein  (25)  and  the  sympathetic 
nerve  (1),  the  site  of  its  subsequent  junction  with  the  independ- 
ently developed  perivenous  lymphatics  of  the  ventral  medias- 
tinal  and  dorsal  prevertebral  regions,  which  together  constitute 
the  anlages  of  this  cephalic  portion  of  the  future  thoracic  duct, 
(cf.  series  143,  slides  x  and  xi,  figs.  172  to  183).  The  thoracic 
duct  approach  ends  blindly  in  section  26  of  slide  vii.  The 


66         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

course  and  the  relations  to  surrounding  structures  of  the  thoracic 
duct  approach  of  this  embryo  are  shown  in  the  dorsal  view  of 
the  reconstruction  (fig.  89),  containing  the  50  sections  of  slide 
vii  in  a  magnification  of  225  diameters. 

This  view  of  the  reconstruction  presents  from  the  lateral  to 
the  mesal  border  the  following  structures. 

1.  Caudal  end  of  left  jugular  lymph  sac,  with  the  jugular  (13) 
and  subclavian  (14)  approaches,  between  which  passes  the  ventral 
branch  of  the  thyro-cervical  artery  (24). 

The  fifth  spinal  nerve  (54)  penetrates  the  lymph  sac,  while 
the  sixth  nerve  lies  on  its  lateral  aspect  with  the  primitive  ulnar 
veno-lymphatic  arching  over  it  to  enter  the  lymph  sac. 

2.  The  dorsal  aspect  of  the  internal  jugular  vein  (25). 

3.  The  main  trunk  and  branches  of  the  thryo-cervical  artery  (24) . 

4.  The  left  superior  intercostal  vein  (46),  with  the  dorsal  (16) 
and  dorso-medial  or  prevertebral  (17)  tributaries,  enters  thedorso- 
medial  angle  of  the  internal  jugular  vein  between  the  thyro- 
cervical  artery  (24)  and 

5.  the  double  strand  of  the  vagus  (22)  and  sympathetic   (l) 
nerves. 

6.  The  thymus  (21). 

7.'  The  aortic  arch  (7),  with  the  left  carotid  artery  (23)  and  the 
origin  of  the  innominate  artery  (45). 

The  thoracic  duct  approach  (12)  arises  by  two  branches  from 
the  dorso-medial  aspect  of  the  sac,  turns  caudo-mesad  between 
the  internal  jugular  vein  and  the  ascending  branch  of  the  thyro- 
cervical  artery,  in  front  of  the  left  superior  intercostal  vein,  and 
approaches  the  recess  formed  between  the  main  vein  and  the 
bundle  of  the  nerves. 

The  reduplication  of  the  origin  of  the  thoracic  duct  approach 
from  the  jugular  lymph  sac  present  in  this  embryo  is  not  unusual, 
and  leads  to  the  type  of  divided  termination  of  the  thoracic  duct 
in  the  adult  shown  in  fig.  56.  The  left  jugular  lymph  sac  (3) 
connects  with  the  venous  system  at  the  common  jugular  angle 
(2)  by  a  larger  ventral  and  smaller  dorsal  jugular  approach  (18). 
It  also  taps  at  the  jugulo-subclavian  angle  (19).  The  thoracic 
duct  enters  the  dorsal  aspect  of  the  sac  by  a  divided  terminal,  the 
lower  branch  connecting  with  the  subclavian  approach. 


DEVELOPMENT  OF  THE  THORACIC  DUCT  67 

Finally  an  intermediate  condition  is  seen  in  another  14  mm. 
embryo,  series  122,  of  which  selected  sections  are  appended,  from 
slides  ix  and  x  (figs.  57  to  62).  Section  21  of  slide  ix  (fig.  57) 
is  taken  at  the  level  where  the  jugular  lymph  sac  has  divided 
for  the  passage  of  the  thyro-cervical  artery  (24)  into  its  two  main 
terminal  components,  viz.,  the  dorsally  placed  subclavian  ap- 
proach (14),  and  the  ventrally  situated  jugular  approach  (13). 
The  latter  appears  in  the  interval  between  the  internal  jugular 
vein  (25)  and  the  jugulo-cephalic  trunk  (29).  These  veins  are 
approaching  each  other  to  form  the  common  jugular  confluence 
(fig.  39,  '26),  at  which  point  the  jugular  approach  usually  makes 
the  secondary  permanent  lymphatico-venous  tap.  The  thoracic 
duct  approach  (12)  arises  from  the  dorsal  aspect  of  the  jugular 
approach  by  a  relatively  narrow  pedicle  and  then  hooks,  as  an. 
elongated  and  expanded  curved  pouch,  ventro-mesad  over  the 
dorsal  aspect  of  the  internal  jugular  vein  towards  the  neuro- 
venous  recess. 

In  section  28  of  the  same  slide  (fig.  58)  the  internal  jugular 
and  jugulo-cephalic  veins  have  met  in  the  common  jugular  con- 
fluence (26)  which  includes  the  jugular  approach.  Consequently 
the  latter  structure  only  appears  in  its  ventral  prolongation  which 
is  seen  occupying  the  ventral  angle  of  the  common  jugular  junc- 
tion (not  labelled  in  fig.  58). 

The  subclavian  approach  (14)  has  moved  relatively  nearer  to 
the  dorsal  surface  of  the  main  vein  channel. 

The  blind  terminal  end  of  the  thoracic  duct  approach  (12)  is 
seen  dorsal  to  the  common  jugular  vein,  between  a  large  dorso- 
medial  tributary  of  the  latter  (16)  mesally,  and  the  thyro-cervical 
artery  (24)  laterally.  Its  pointed  extremity  is  directed  further 
ventro-mesad  toward  the  interval  between  the  sympathetic  nerve 
(1)  and  the  medial  surface  of  the  common  jugular  vein  (26). 

In  section  7  of  slide  x  (fig.  59)  the  terminal  of  the  thoracic 
duct  approach  (12)  has  relatively  receded  and  lies  in  the  narrow 
interval  between  thyro-cervical  artefy  (24)  and  common  jugular 
vein  (26). 

In  fig.  60  (section  9  of  slide  x)  a  large  dorso-medial  venous 
tributary  (16,  left  superior  intercostal  vein)  empties  into  the 


68          DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC   VESSELS 

dorso-medial  angle  of  the  common  jugular  trunk.  The  thoracic 
duct  approach  (12),  occupying  the  same  relative  position  as  in  the 
preceding  figure,  lies  between  this  tributary  and  the  thyro-cer- 
vical  artery,  dorsal  to  the  main  vein.  Section  12  of  slide  x  (fig. 
61)  shows  the  distal  reduced  end  of  the  approach  in  this  same 
situation.  The  subclavian  approach  of  the  jugular  lymph  sac 
(14)  is  reduced  to  a  narrow  longitudinal  cleft  on  the  dorso-lateral 
aspect  of  the  main  vein.  This  reduction  is  coincident  with  the 
derivation  from  the  dorsal  aspect  of  the  subclavian  approach  of 
the  primitive  ulnar  veno-lymphatic  (31).  This  channel  arches 
dorsad  over  the  Vlth  spinal  nerve  (30),  and  appears  in  this  sec- 
tion in  its  typical  relation  to  this  nerve.  Finally  in  the  succeed- 
ing section,  13  of  slide  ix,  (fig.  62),  the  thoracic  duct  approach 
ends  blindly.  The  structures  shown  in  the  section  dorsal  to 
the  common  jugular  trunk  are  now  encountered  in  the  following 
order:  mesally  the  terminal  of  one  of  the  branches  of  the  dorso- 
medial  venous  plexus  (16)}  next  the  thyro-cervical  artery  (24)} 
then  the  Vlth  segmental  nerve  (30),  and,  dorsal  of  this,  the 
primitive  ulnar  veno-lymphatic  (31). 

The  series  of  sections  of  this  embryo  shown  here  are  interest- 
ing not  only  in  respect  to  the  behavior  of  the  thoracic  duct 
approach,  but  also  in  reference  to  the  mutual  relations  of  this 
structure  and  the  terminals  of  the  dorso-medial  tributary  venous 
plexus.  These  relations  are  to  be  discussed  subsequently  in  con- 
sidering, as  whole,  the  evidence  upon  which  some  investigators 
have  based  their  conception  of  direct  venous  origin  of  the  lym- 
phatic system  by  fusion  of  a  number  of  separate  elements  de- 
tached from  the  main  venous  trunks  (cf.  infra  p.  153.) 

The  variable  appearance  of  the  thoracic  duct  approach  in  the 
younger  stages  is  perhaps  best  illustrated  by  the  exaggerated 
development  presented  in  a  13  mm.  embryo  (series  92),  in  which 
the  process  occupies  the  last  thirteen  sections  of  slide  x,  and  the 
first  fourteen  sections  of  slide  ix.  Selected  microphotographs 
of  this  series  are  shown  in  figs.  63  to  78.  The  embryo  presents 
the  largest  and  most  dilated  thoracic  duct  approach  of  any  in  my 
collection.  Fig.  63  gives  a  topographical  view  of  the  region 
involved.  The  succeeding  sections  are  cut  down  and  confined 


DEVELOPMENT  OF  THE  THORACIC  DUCT          69 

to  the  immediate  neighborhood  of  the  thoracic  duct  approach. 
Fig.  63  shows  the  sections  of  the  internal  jugular  vein  (25)  and 
jugulo-cephalic  trunk  (29),  approaching  their  point  of  union  in 
the  common  jugular  confluence.  A  large  process  of  the  jugular 
lymph  sac  (13)  extends,  as  the  jugular  approach,  into  the  interval 
between  the  main  veins.  Along  the  mesal  aspect  of  the  internal 
jugular  vein  (25). are  placed  the  sympathetic  (1),  the  vagus  (22), 
the  left  common  carotid  artery  (28),  and,  further  ventrad,  the 
thymus  (21 ) .  The  dorsal  portion  of  the  sac  is  about  to  form  the 
subclavian  approach  (11,  14). 

In  fig.  64,  the  jugular  approach  (13)  has  entered  more  deeply 
into  the  narrowing  interval  between  the  internal  jugular  (25) 
and  jugulo-cephalic  trunks  (29),  and  the  sharply  marked  con- 
striction between  it  and  the  remainder  of  the  sac  (subclavian 
approach,  14)  foreshadows  its  coming  separation  from  the  latter. 
A  protrusion  of  the  dorso-medial  angle  of  the  jugular  approach, 
adjacent  to  the  internal  jugular  vein,  indicates  the  beginning 
derivation  of  the  thoracic  duct  approach  (12). 

In  the  succeeding  section  (fig.  65)  the  jugular  approach  (13) 
has  separated  from  the  subclavian  approach  (14)  of  the  jugular 
lymph  sac  and  thus  cleared  the  path  for  the  passage  of  the  thyro- 
cervical  artery  (24)  between  the  two  cardinal  divisions  of  the 
lymph  sac,  whose  caudal  terminations  are  represented  by  the 
jugular  and  subclavian  approaches.  The  origin  of  the  thoracic 
duct  approach  (12)  from  the  dorso-medial  angle  of  the  jugular 
approach  is  now  defined. 

In  the  succeeding  section  (fig.  66)  the  triple  termination  of  the 
jugular  lymph  sac,  in  the  subclavian  (14),  jugular  (13)  and  tho- 
racic duct  approaches  (12),  is  accomplished,  and  the  latter  is  begin- 
ning to  extend  mesad  across  the  dorsal  surface  of  the  internal 
jugular  vein.  The  main  thyro-cervical  artery  is  approaching 
the  junction  with  its  secondary  dorsal  branches. 

In  fig.  67  the  jugular  approach  (13)  has  divided  into  the  inter- 
mediate part  between  the  internal  (25)  and  jugulo-cephalic  (29) 
veins,  which  is  to  establish  the  tap  at  the  common  jugular  angle, 
and  a  ventral  process  which  extends  from  the  tap  caudad  over 
the  ventral  surface  of  the  common  jugular  angle  and  vein. 


70         DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

The  thoracic  duct  approach  has  enlarged,  is  partially  subdivided 
(cf.  p.  65,  figs.  48  and  49,  series  189)  and  its  blind  terminal 
extremity  is  reaching  ventro-mesad  into  the  angle  between  internal 
jugular  vein  and  sympathetic  (7).  The  thyro-cervical  artery  (24) 
lies  between  the  subclavian  and  thoracic  duct  approaches,  dorsal 
to  the  jugulo-cephalic  trunk  (29). 

In  fig.  68  the  thoracic  duct  approach  has  further  enlarged  and 
is  still  subdivided  into  two  compartments  the  terminal  of  which 
abuts  directly  against  the  sympathetic  nerve.  The  jugular 
approach  (13)  communicates  in  this  section  with  the  internal 
jugular  vein,  while  a  narrower  slit-like  division  continues  further 
caudad  toward  the  common  jugular  angle. 

In  fig.  69  the  internal  (25)  and  jugulo-cephalic  (29)  trunks  are 
only  separated  from  each  other  by  a  narrow  septum  containing 
the  lumen  of  the  slit-like  prolongation  of  the  jugular  approach. 
Both  in  this  and  in  the  preceding  section  the  ventral  process  of 
the  jugular  approach  lies  in  the  angle  between  the  two  veins, 
closely  applied  to  their  ventral  surface. 

The  thoracic  duct  approach  is  a  large  sausage-shaped  structure, 
curved  over  the  dorsal  surface  of  the  internal  jugular  vein.  The 
septum  in  its  interior  has  disappeared  and  the  process  presents  a 
clear  lumen. 

In  fig.  70  (slide  ix,  section  2),  the  confluence  of  internal  jugular 
and  jugulo-cephalic  trunks  has  taken  place  (26).  The  thoracic 
duct  approach  (12)  has  extended  both  ventro-mesad  into  an  area 
of  indifferently  defined  mesodermal  spaces,  mesad  to  the  sym- 
pathetic nerve  (1),  and  laterad  toward  the  subclavian  approach 
of  the  jugular  sac  (14),  passing  between  common  jugular  vein 
(26)  and  thyro-cervical  artery  (24)> 

In  section  5  of  slide  ix  (fig.  71)  the  thoracic  duct  approach 
(12)  appears  as  a  long  curved  multilocular  channel,  which  laterad 
reaches  the  subclavian  approach  of  the  jugular  lymph  sac,  between 
the  thryo-cervical  artery  (24)  and  common  jugular  vein  (26), 
while  its  blind  mesal  extremity  terminates  just  dorsal  to  the  sym- 
pathetic-vagus strand.  In  the  following  section  (fig.  72)  the 
thoracic  duct  approach  (12)  connects  with  the  subclavian  approach 
(14)  of  the  jugular  lymph  sac  affording  an  instance  of  the  gene- 


DEVELOPMENT  OF  THE  THORACIC  DUCT  71 

sis  of  the  reduplicated  or  multiple  thoracic  duct  terminations  oc- 
casionally encountered  in  the  adult  as  above  described  (cf.p.  66, 
fig.  56,  series  212,  slide  ix,  figs.  34  to  42). 

In  fig.  73  (series  92,  slide  ix,  section  9)  the  subclavian  approach 
(14)  is  much  reduced,  and  lies  along  the  lateral  aspect  of  the  com- 
mon jugular  vein  '(26).  Its  connection  with  the  thoracic  duct 
approach  (12)  is  plainly  visible,  passing  between  the  main  vein 
(26)  and  the  thyro-cervical  artery  (24).  Dorsal  somatic  and 
prevertebral  venous  tributaries  (16),  approaching  the  dorso- 
medial  angle  of  the  common  jugular  vein  (26),  intersect  the  course 
of  the  thoracic  duct  approach,  and  begin  to  divide  the  same  into 
a  medial  and  a  lateral  element.  This  division  is  completed  in 
the  following  section  (fig.  74)  in  which  the  united  dorsal  and  pre- 
vertebral tributaries  form  a  venous  trunk  of  considerable  size 
(16)  which  is  approaching  its  confluence  with  the  common  jugular 
vein  by  passing  between  the  lateral  and  medial  components  of 
the  thoracic  duct  approach.  In  other  words,  the  appearance  of 
the  thoracic  duct  approach  in  this  and  in  the  following  sections 
is  the  expression  of  the  ventro-mesal  arched  course  of  this  structure 
across  the  fork  or  angle  between  the  common  jugular  vein  (26)  and 
the  terminal  of  its  ventro-medial  tributary  plexus  (16).  The  recon- 
structions shown  in  figs.  89,  90  and  91  indicate  this  topographical 
relationship  clearly.  The  blind  mesal  end  of  the  arched  process 
(12)  now  lies  mesal  to  the  tributary  vein  (16)  and  dorsal  to  the 
sympathetic  nerve  (1).  In  the  following  section  (section  11  of 
slide  ix,  fig.  75),  the  dorso-medial  venous  tributary  (16)  is  elong- 
ated and  close  to  the  main  vessel,  while  the  reduced  sections  of 
the  thoracic  duct  approach  lie  on  either  sid«  of  the  same,  as  indi- 
cated by  the  forked  leader  (12).  The  subclavian  approach  (14), 
still  prominent  and  connected  with  the  medial  section  of  the 
thoracic  duct  approach  in  the  preceding  section  10  (fig.  74), 
appears  now  in  section  1 1  reduced  to  a  detached  small  blind  end 
(not  labelled  in  the  figure),  close  to  the  lateral  wall  of  the  main 
vein  and  ventral  to  the  thyro-cervical  arterj^  (24)-  In  the  suc- 
ceeding section  12  (fig.  76)  the  dorso-medial  venous  tributary 
(superior  intercostal  vein)  enters  the  common  jugular  trunk. 
The  lateral  portion  of  the  thoracic  duct  approach  (not  labelled 


72        DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC   VESSELS 

in  the  figure)  is  seen  in  the  deep  recess  between  this  entrance, 
the  main  vein  (26}  and  the  thyro-cervical  artery  (24} .  The  mesal 
end  of  the  thoracic  duct  approach  terminates  blindly  in  this 
section  just  dorsal  to  the  sympathetic  nerve  (!}.  In  section  13 
(fig.  77)  the  lateral  terminal  of  the  thoracic  duct  approach  (12} 
can  still  be  clearly  seen  in  the  interval  between  the  wide  dorsal 
opening  of  the  combined  somatic  and  prevertebral  (17}  tributary 
stem  into  the  main  vein  (26}  and  the  thyro-cervical  artery  (24}> 
It  appears  very  much  reduced  in  the  same  situation  in  section 
14  (fig.  78),  and  ends  blindly  in  the  following  section.  The  last 
three  sections  of  this  series  (figs.  76,  77  and  78)  show  the  begin- 
ning of  the  jugulo-subclavian  confluence. 

In  the  later  stages  the  thoracic  duct  approach  has  extended 
further  ventro-mesad  into  the  recess  between  the  common  jugular 
vein  and  the  sympathetic  nerve,  and  in  this  situation  it  eventually 
makes  its  connection  with  the  two  independently  developed  lym- 
phatic channels  of  the  anterior  mediastinal  region,  viz.,  the 
preazygos  segment  of  the  thoracic  duct  dorsally,  and  the  broncho- 
mediastinal  trunk  ventrally.  The  mode  of  this  union  is  dis- 
cussed below  under  a  separate  heading  (cf.  infra,  p.  111).  Figs. 
79  to  82  show  transverse  sections  of  the  left  side  of  the  lower 
cervical  region  in  a  15  mm.  cat  embryo  (series  245,  slide  xi, 
sections  24  to  27,  X  225),  and  fig.  90  gives  the  dorsal  view  of  the 
reconstruction  on  the  same  scale  of  the  thoracic  duct  approach 
and  the  related  structures  in  the  same  embryo  (slide  xi,  sections 
1-44).  In  fig.  79  (slide  xi,  section  24)  the  terminal  extremity 
of  the  thoracic  duct  approach  (12}  is  seen  between  the  common 
jugular  vein  (26}  and  the  sympathetic  nerve  (!},  having  reached 
this  situation  by  extending  ventro-mesad  across  the  dorsal  tribu- 
tary 16  (left  superior  intercostal  vein),  between  this  vessel  and 
the  main  venous  trunk. 

The  section  is  taken  below  the  common  jugular  confluence, 
consequently  the  jugular  approach  is  no  longer  seen,  and  the 
blind  end  of  the  thoracic  duct  approach  appears  isolated.  The 
only  other  portion  of  the  jugular  lymph  sac  carried  caudad  to  this 
level  is  the  subclavian  approach  (14),  seen  on  the  lateral  aspect 
of  the  main  vein.  The  sequence  of  structures  now  successively 


DEVELOPMENT  OF  THE  THOKACIC  DUCT  73 

encountered  along  the  mesal  and  dorsal  aspects  of  the  main  com- 
mon jugular  vein  (26}  are  the  following,  proceeding  meso-laterad : 

1.  Thymus  (21),  with  sub-  and  suprathymic  venous  tributaries 
entering  the  main  vein. 

2.  Left  common  carotid  artery  (23). 

3.  Vagus  nerve  (22). 

4.  Sympathetic  nerve  (1). 

5.  Thoracic  duct  approach  (12). 

6.  Dorsal   somatic   tributary  of  main  vein  (16).     (Anlage  of 
left  superior  intercostal  vein). 

7.  Thyro-cervical  artery  (24). 

8.  Subclavian   approach  of  jugular  lymph  sac   (14),   on  the 
dorso-lateral  aspect  of  the  common  jugular  vein. 

This  order  and  relationship  is  maintained  uniformly  and  clearly 
in  the  three  succeeding  sections  shown  in  f  gs.  80,  81  and  82. 

In  the  last  of  these  the  dorsal  venous  tributary  (16)  enters  the 
main  common  jugular  channel. 

The  sections  can  be  easily  followed  and  oriented  by  reference 
to  the  dorsal  view  of  the  reconstruction  shown  in  fig.  90.  The 
same  is  composed  of  the  plates  of  all  44  sections  of  slide  ix  of  series 
245.  In  this  embryo  the  thoracic  duct  approach  has  already 
established  its  definite  and  permanent  connection  with  the  inde- 
pendently developed  channel  of  the  preazygos  segment  of  the 
thoracic  duct  (35,  in  fig.  90),  as  described  in  detail  below  (cf. 
p.  111).  The  point  of  this  junction  is  indicated  in  the  reconstruc- 
tion by  the  narrowing  of  the  two  spindles  12  and  35  (thoracic 
duct  approach  and  preazygos  segment  of  thoracic  duct)  to  form 
an  isthmus  situated  just  cephalad  of  the  leader  marked  16-46. 

The  reconstruction  includes  the  terminal  of  the  jugular  ap- 
proach (13),  with  the  origin  from  the  same  of  the  thoracic  duct 
approach  (12),  and  the  entire  subclavian  approach  (14)  of  the 
jugular  lymph  sac.  The  ventral  division  of  the  thyro  cervical 
artery  (24)  passes  forward  between  the  jugular  and  subclavian 
approaches  of  the  lymph  sac,  accompanied  by  a  vein  (not  labelled 
in  the  figure)  which  is  constantly  found  in  this  situation  in  the 
adult,  draining  from  the  prevertebral  area  into  the  common 
jugular  trunk. 


74         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

The  dorsal  and  dorso-medial  venous  tributary  plexus  has 
united  into  the  stem  of  the  left  superior  intercostal  vein  (16-4-6}. 
The  reconstruction  shows  well  .the  caudo-mesal  turn  of  the 
thoracic  duct  approach  (12)  in  the  fork  between  the  main  vein  (26) 
and  the  superior  intercostal  (16-46),  accompanied  by  the  mesal 
branch  of  the  thyro-cervical  artery.  The  terminal  of  the  thor- 
acic duct  approach  (12)  meets  and  unites  with  the  preazygos 
segment  of  the  thoracic  duct  (35)  on  the  mesal  shoulder  of  the 
superior  intercostal  vein  terminal,  between  it  and  the  sympathetic 
nerve  (1).  This  is  one  of  the  two  types  of  topographical  relation- 
ship encountered  (cf.  infra  pp.  75,  76).  Further  laterad  follow 
the  vagus  (22)  and  the  sympathetic  strand  (1),  intersecting  at  an 
acute  angle.  Then  the  left  common  carotid  artery  (23)  and  the 
thymus  (21)  with  the  perithymic  venous  plexuses. 

Figs.  83  to  8,8  show  the  caudal  end  of  the  left  jugular  lymph 
sac  and  the  thoracic  duct  approach  in  a  selected  series  of  sections 
from  a  17  mm.  cat  embryo  (series  142),  all  magnified  225  diame- 
ters, and  fig.  91  gives  the  dorsal  view  of  the  reconstruction  of 
this  region  from  the  same  embryo. 

These  preparations  are  introduced  here  for  the  purpose  of 
illustrating,  in  comparison  with  the  preceding  series  (245)  the 
second  type  of  relationship  which  the  thoracic  duct  approach 
may  bear  to  the  combined  vagus-sympathetic  strand. 

Fig.  83  (series  142,  slide  x,  section  13)  shows  the  transection 
of  the  caudal  end  of  the  left  jugular  lymph  sac  in  the  interval 
between  the  internal  jugular  (25)  and  jugulo-cephalic  (29)  veins 
which  are  approaching  their  confluence  to  form  the  common 
jugular  trunk. 

The  form  of  the  jugular  lymph  sac  already  indicates  its  coming 
division  into  the  three  terminal  " approaches,"  the  jugular  ap- 
proach (14),  the  subclavian  approach  (13)  and  the  thoracic  duct 
approach  (12).  The  latter  covers  the  entire  dorsal  circumference 
of  the  internal  jugular  vein  (25)  and  its  termination  points  to  the 
angular  recess  between  the  sympathetic  (1)  and  vagus  (22). 
Ventrad  to  the  latter  the  field  includes  the  thymus  (21).  The 
thyro-cervical  artery  is  cut  in  several  of  its  divisions,  two  of  which 
are  indicated  by  the  forked  leader  24- 


DEVELOPMENT  OF  THE  THORACIC  DUCT          75 

In  fig.  84  (series  142,  slide  x,  section  16),  the  subclavian  ap- 
proach (14)  has  separated  from  the  jugular  approach  (13)  and 
the  thyro-cervical  artery  (24)  is  passing  meso-laterad  between 
these  two  divisions.  The  origin  of  the  thoracic  duct  approach 

(12)  from  the  dorso-medial  circumference  of  the  jugular  approach 

(13)  is  well  shown  in  the  section.     The  concavity  of  the  jugulo- 
cephalic  arch  is  expressed  by  the  two  cross-sections  labelled  29. 

In  fig.  85  (series  142,  slide  x,  section  8)  the  thoracic  duct 
approach  (12)  has  separated  from  the  jugular  approach  (18). 
The  curve  of  the  process,  with  the  concavity  directed  meso- 
caudad,  gives  the  two  cross  sections  of  its  lumen  included  in  the 
forked  leader  12.  The  termination  of  the  thoracic  duct  approach 
has  still  further  invaded  the  recess  between  sympathetic  (1)  and 
vagus  (22)  and  a  slight  interval  has  developed  between  the  two 
nerves. 

The  lateral  circumference  of  the  vagus  (22)  covers  practically 
the  entire  mesal  aspect  of  the  internal  jugular  vein  (25). 

In  the  following  figure  (fig.  86,  series  142,  slide  x,  section  20) 
the  termination  of  the  thoracic  duct  process  (12)  is  seen  slipping 
through  the  interval  between  sympathetic  (1 )  dorsally  and  vagus 
(22)  ventrally.  Instead  6f  lying  therefore  dorso-lateral  to  the 
sympathetic — as  in  the  preceding  series  245 — the  end  of  the 
thoracic  duct  approach  in-  the  present  instance  passes  mesad  on 
the  ventral  aspect  of  this  nerve,  between  the  same  and  the  vagus. 
This  relationship  is  also  seen  in  the  two  succeeding  figures,  87 
and  88  (series  142,  slide  x,  sections  22  and  24.) 

We  are  dealing  therefore  apparently  with  two  potential  paths 
which  the  blind  terminal  of  the  thoracic  duct  approach  may  take 
in  its  passage  from  the  jugular  lymph  sac  mesad  beyond  the  vagus- 
sympathetic  line  to  the  upper  mediastinal  region,  where  it  estab- 
lishes eventually  its  secondary  connections  with  the  preazygos 
segment  of  the  thoracic  duct  and  with  the  broncho-mediastinal 
trunk.  In  one  type  (illustrated  by  the  sections  and  reconstruc- 
tions of  series  245  (figs.  79  to  82,  fig.  90)  the  process  dips,  after 
passing  between  the  left  superior  intercostal  and  main  jugular 
vein  at  an  acute  angle,  caudad  on  the  lateral  side  of  the  sympa- 
thetic strand  (fig.  90). 


76        DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

In  the  other  type,  illustrated  by  series  142  (figs.  83  to  88;  fig. 
91)  the  thoracic  duct  approach,  maintaining  the  identical  relation 
to  left  superior  intercostal  and  common  jugular  veins,  gains  the 
ventro-medial  aspect  of  the  sympathetic  cord,  by  passing  ob- 
liquely between  the  same  and  the  vagus. 

In  schematic  cross  section  these  two  conditions  may  be  illus- 
trated by  the  accompanying  text  figures: 


In  regard  to  the  remaining  structures  fig.  87  (series  142,  slide 
X,  section  22)  shows,  by  comparison  with  the  preceding  figure 
86,  the  tap  of  the  jugular  approach  into  the  internal  jugular  vein 
(25}  just  above  the  confluence  with  the  jugulo-cephalic  trunk 
(29],  and  the  prolongation  of  its  ventral  process  (13)  over  the 
ventral  aspect  of  the  common  jugular  angle.  Fig.  88  (series  142, 
slide  X,  section  24)  shows  the  confluence  of  the  internal  jugular 
(25)  and  jugulo-cephalic  (29)  veins  fully  established,  and  gives 
a  very  clear  picture  of  the  relation  which  the  ventral  prolongation 
(13)  from  the  jugular  approach  of  the  lymph  sac  bears  to  the 
common  jugular  angle.  In  both  figs.  87  and  88  the  dorsal  venous 
tributary  (sup.  intercostal  vein  anlage)  is  indicated  by  the 
leader  16.  It  enters  the  main  vein  in  section  3  of  the  following 
slide  (xi).  Fig.  91  gives  the  dorsal  view  of  the  reconstruction 
of  the  vascular  and  nervous  structures  of  the  left  side  in  slides 


DEVELOPMENT  OF  THE  THORACIC  DUCT  77 

x  and  xi  of  this  embryo,  carried  caudad  to  the  level  of  the  verte- 
bral vessels  (41,  4®)-  Comparison  with  fig.  90  will  show  the 
correspondence  of  the  two  preparations  in  all  essential  points  and 
will  accentuate  the  above  described  difference  in  the  course  of 
the  thoracic  duct  approach  (12}  and  the  preazygos  segment  of 
the  thoracic  duct  (85}  in  relation  to  the  vagus-sympathetic  strand. 

It  is  readily  seen,  in  comparing  the  reconstructions  of  the  two 
older  stages  just  described  (figs.  90  and  91)  with  that  of  the 
earlier  embryo  shown  in  fig.  89,  that  the  latter,  in  the  construction 
of  the  terminal  of  its  thoracic  duct  approach,  combines  poten- 
tially the  ability  of  developing  into  either  one  of  the  two  more 
advanced  conditions  just  described.  The  process  which  the 
thoracic  duct  approach  turns  nearly  horizontally  mesad  into  the 
interval  between  vagus  and  sympathetic  is  present  in  all  three 
reconstructions.  In  many  embryos,  as  will  appear  presently  in 
describing  the  critical  stages  in  detail,  the  thoracic  duct  approach 
appears  to  make  its  connection  with  the  independently  developed 
anlages  of  the  preazygos  portion  of  the  thoracic  duct  in  this  situa- 
tion, and  continued  development  will  lead  to  the  condition  seen  in 
series  142  (fig.  91).  If,  on  the  other  hand,  the  caudal  extremity 
of  the  thoracic  duct  approach  of  the  13.5  mm.  embryo  (fig.  89) 
joins  the  independently  developed  lymphatic  anlages  at  the  root 
of  the  left  superior  intercostal  vein  and  along  the  common  jugular 
lateral  to  the  sympathetic  line,  the  resulting  relation  will  be  as  seen 
in  series  245  (fig.  90). 

These  observations  are  further  supported  by  comparison  of  the 
preparations  just  described  with  the  corresponding  portions  of 
the  two  reconstructions  shown  in  figs.  170  and  171. 

Fig.  170  (series  218)  shows  the  stage  in  a  15  mm.  embryo  just 
prior  to  the  junction  of  the  thoracic  duct  approach  with  the  inde- 
pendently formed  preazygos  segment  of  the  thoracic  duct  (35}. 
The  latter  is  in  its  greater  part  already  a  distinct  and  considerable 
segment  of  the  future  continuous  duct  channel.  Between  its 
blind  cephalic  extremity  and  the  blind  caudal  end  of  the  thoracic 
duct  approach  (12}  are  a  number  of  scattered  and  still  separate 
lymphatic  anlages  along  the  common  jugular  and  innominate 
veins  on  each  side  of  the  sympathetic  line.  By  continued  exten- 


78         DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

sion  of  these  as  yet  isolated  lymphatic  anlages  the  still  lacking 
intermediate  bondpiece  will  be  produced,  which,  by  union  of  its 
cephalic  extremity  with  the  thoracic  duct  approach  of  the  jugular 
lymph  sac  and  junction  of  its  caudal  end  with  the  cephalh  ternrnnl 
of  the  preazygos  segment  of  the  thoracic  duct  (35),  will  produce 
the  continuous  and  uninterrupted  lymph  channel  of  the  succeed- 
ing stage  (se:ies  143,  15.5  mm.  embryo,  fig.  171).  A  study  of  the 
reconstruction  of  series  218  makes  it  evident  that  the  opportunity 
still  exists  of  developing  this  final  junction  either  on  the  dorso- 
lateral  or  ventro-medial  side  of  the  sympathetic  cord,  for  the 
lymphatic  anlages  exist  in  both  situations.  The  end  of  the 
thoracic  duct  approach  of  this  embryo  rides  with  a  well  marked 
lateral  and  medial  prolongation  in  the  fork  formed  by  the  en  trance 
of  the  left  superior  intercostal  vein  (16-4-6}  into  the  common 
jugular.  The  lateral  process,  carrying  the  leader  12  in  the  figure, 
is  in  position  to  join  the  line  of  separate  lymphatic  anlages  extend- 
ing caudad  on  the  lateral  side  of  the  sympathetic,  and  a  prominent 
cephalic  process  of  the  already  established  segment  of  the  preazy- 
gos lymph  channel  extends  cephalo-laterad  across  the  dorsal 
surface  of  the  nerve,  as  if  to  meet  the  lymphatic  line  just  described. 
If  development  had  proceeded  along  this  line  in  this  embryo,  the 
condition  seen  i.n  series  245  might  have  resulted,  with  the  modifi- 
cation of  swinging  the  thoracic  duct  approach  to  the  lateral 
instead  of  to  the  medial  side  of  the  left  superior  intercostal  vein, 
but  carrying  the  thoracic  duct  along  the  dorso-lateral  aspect 
of  the  sympathetic  nerve.  In  this  case  the  large  separate  lym- 
phatic anlage  labelled  35'  in  fig.  170  would  take  an  important 
share  in  building  up  the  resulting  lymph  channel.  On  the  other 
hand,  the  definite  connection  with  the  preazygos  segment  of  the 
thoracic  duct  might  have  been  established  through  the  ventro- 
medial  terminal  prolongation  of  the  thoracic  duct  approach.  A 
piece  of  the  sympathetic  nerve  has  been  removed  in  the  recon- 
struction in  order  to  show  the  position  of  this  structure,  in  the 
interval  between  sympathetic  nerve  (1)  and  vagus  (22).  The 
long  slender  prolongation  extending  forward  between  vagus  (22) 
and  common  carotid  artery  (23)  is  the  path  of  junction  for  the 
ventral  or  broncho-mediastinal  lymphatic  trunk.  I  am  under 


DEVELOPMENT  OF  THE  THORACIC  DUCT  79 

the  strong  impression  that  the  observed  variations  in  the  relation 
of  the  embryonic  thoracic  duct  approach  to  the  sympathetic 
nerve  hinge  largely  for  their  production  upon  the  share  which 
the  broncho-mediastinal  duct  is  to  take  in  individual  cases  in 
the  establishment  of  the  preazygos  segment  of  the  thoracic  duct 
channel.  (Compare  relations  of  35  and  37  in  the  schematic 
cross  sections  shown  above  in  the  text  figures.) 

If  now  this  ventro-medial  end  piece  of  the  thoracic  duct 
approach  had  effected  its  junction  with  the  preazygos  segment  of 
the  thoracic  duct  along  the  line  of  the  lymphatic  anlages  on  the 
medial  side  of  the  sympathetic  and  in  the  interval  between  this 
strand  and  the  vagus,  then  the  individual  condition  already  de- 
scribed in  series  142  (fig.  91)  would  have  resulted. 

This  same  topographical  relationship  of  sympathetic  nerve  and 
lymph  channel  is  also  seen  in  the  15.5  mm.  embryo,  series  143, 
shown  in  reconstruction  from  the  right  side  in  Fig.  171.  The 
thoracic  duct  approach  (12)  intersects  the  sympathetic  nerve  (1) 
on  its  ventro-medial  aspect  at  an  acute  angle  to  establish  its  con- 
nection with  the  cephalic  end  of  the  preazygos  segment  of  the 
thoracic  duct  (35).  This  type  appears  the  prevalent  one  in  the 
embryos  in  my  collection. 

I  am  strongly  inclined,  on  the  evidence  of  the  embryos  of  my 
collection,  to  regard  the  development  of  the  thoracic  duct  approach 
of  the  jugular  lymph  sac  as  occupying  three  distinct  chronological 
stages : 

1.  Early  stage.    Embryos  of  13-13.5  mm. 

Series     92—13.   mm. 
Series  189—13.5  mm. 

In  this  period  the  thoracic  duct  approach  appears  large,  at 
times  multilocular,  and  shares  the  redundancy  and  capacious 
lumen  which  characterizes  the  entire  jugular  lymph  sac  in  the 
earlier  genetic  period. 

2.  Intermediate  stage.     Embryos  of  14  mm. 

Series  210 — 14   mm. 
Series  212—14  mm. 
Series  122—14  mm. 
The  sac,  as  a  whole,  and  the  thoracic  duct  approach  in  particu- 


80    DEVELOPMENT  OF  THE  SYSTEMIC  LYMPHATIC  VESSELS 

lar,  condenses  and  becomes  more  clearly  defined  against  the  sur- 
rounding mesoderm.  The  multilocular  character  due  to  rem- 
nants of  the  capillary  walls  in  the  interior,  disappears  and  the 
approach  obtains  a  clear  and  clean-cut  lumen.  The  entire  struc- 
ture appears  to  contract  somewhat  on  itself  and  develops  more 
distinct  walls.  The  recession,  during  which  the  thoracic  duct 
approach  occupies  a  relatively  smaller  territory  is  succeeded  by 
3.  Final  stage.  Embryos  of  15-17  mm. 

Series  245 — 15  mm. 

Series  218 — 15  mm. 

Series  143 — 15.5  mm. 

Series  142 — 17  mm. 

In  this  period  the  sac,  through  its  digitate  processes,  establishes 
the  definite  connections  with  the  independently  formed  systemic 
extraintimal  lymphatic  channels.  Specifically  the  thoracic  d  uct 
approach  of  the  sac  unites  secondarily  with  the  preazygos  seg- 
ment of  the  thoracic  duct  and  with  the  broncho-mediastinal 
lymphatic  trunk. 

While  I  do  not  insist  on  the  above  outlined  details  in  the 
chronological  order  of  development  of  the  thoracic  duct  approach, 
the  embryos  of  my  collection  certainly  tend  to  support  the  view 
expressed.  Thus  the  13  mm.  embryo  (series  92)  offers  the 
highest  degree  of  expansion  of  the  thoracic  duct  approach.  The 
structure  recedes  and  diminishes  somewhat  in  extent  in  the 
13.5  mm.  stage  (series  189),  appears  uniformly  further  reduced 
and  shortened  in  the  14  mm.  embryos  (series  210,  212,  122),  and 
finally,  from  the  15  and  15.5  mm.  stages  on,  makes  its  definite 
connections  with  the  preformed  independently  developed  chan- 
nels of  the  thoracic  and  broncho-mediastinal  ducts. 

In  this  entire  genetic  process  there  is  not  the  slightest  indica- 
tion of  an  extension  of  lymphatic  trunks  from  the  jugular  sac  or 
from  its  thoracic  duct  approach  toward  the  periphery.  There 
is  absolutely  no  suggestion  of  so-called  "  budding"  or  "  sprout- 
ing," or  of  any  other  form  of  centrifugal  extension  of  lymphatic 
vessels.  On  the  contrary,  the  sac  as  a  whole,  and  the  processes 
therewith  connected,  recede  actually  for  a  time,  and  only  then 
establish  a  secondary  junction  with  the  independently  developed 


DEVELOPMENT  OF  THE  THORACIC  DUCT  81 

general  systemic  lymphatic  channels.  These  have  in  the  mean- 
while formed  along  and  around  the  temporary  embryonic  veins, 
as  the  result  of  the  confluence  of  large  numbers  of  extraintimal 
perivenous  spaces  in  the  sense  previously  defined  in  detail. 
Their  line  of  further  growth,  extension  and  union  with  each  other 
is  altogether  centripetal,  from  the  outlying  regions  toward  the 
jugular  lymph  sacs,  and  their  union  with  the  latter's  processes 
is  the  last  and  final  step  in  the  definite  organization  of  the  lym- 
phatic system. 


PART  II,  PLATES 

FIGURES  29  TO  91 


FIGURE  29 

29  Color  schema,  showing  the  four  genetic  segments  of  the  thoracic  ducts  (I, 
II,  III,  IV)  in  the  cat,  and  their  relations  to  the  embryonal  veins,  the  broncho- 
mediastinal  trunk  (37),  and  the  jugular  lymph  sacs  (II). 

3'  Precardinal  or  precava  of  right  side. 

3  Right  azygos  vein,  thoracic  portion. 

6  Precardinal  or  precava  of  left  side. 
6'  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

11  Jugular  lymph  sac. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

26  Common  jugular  vein. 

27  External  jugular  vein. 

28  Cephalic  vein. 

33  Subclavian  artery. 

33'  Subclavian  vein. 

35  Thoracic  duct,  preazygos  segment. 

36  Thoracic  duct,  azygos  segment. 

37  Broncho-mediastinal  duct. 
40  Innominate  vein. 

46  Left  superior  intercostal  vein. 

52  Postazygos  segment  of  thoracic  duct. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  22 


27 


28 


IV. 


MEMOIR  NO.   1,  HUNTINGTON,   1911 


29 


FIGURES  30  AND  31 

30  Transverse  section  through  left  side  of  lower  cervical  region  in  a  14  nun.  cat 
embryo  (series  210,  slide  VIII,  section  39) ,  X  225. 

31  Same,  section  40. 

1    Sympathetic  nerve. 

11  Jugular  lymph  sac. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus. 

18  Peritracheal  venous  plexus. 

19  Suprathymic  venous  plexus. 

20  Subthymic  venous  plexus. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 


THK   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   23 


16 


18 


25 


MEMOIR   NO.   1,   HUNTINGTON,    1911 


FIGURES  32,  33  AND  34 

32  Same,  section  41. 

33  Same,  section  42. 

34  Transverse  section  through  left  side  of  lower  cervical  region  in  a  14  mm.  cat 
embryo  (series  212,  slide  IX,  section  24),  X  200. 

1  Sympathetic  nerve. 

8  Oesophagus. 

11  Jugular  lymph  sac. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus. 

18  Peritracheal  venous  plexus. 
22  Vagus. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   24 


>;V-v']r:.->.-"f*>//»^a^  *•$.    •* 


.*. .  •  .*^^*.<hgLKj.*.'-  a' «»«  • .  ^  ^  -\ 


18 


24 


11 


12 


25 


'/    ^  *  >     *.  •*          £^A  "  **  *         «-•      ^.  ,       "      1      *'•%£& 

^'i  '  ,-  v.'.'  '•  -vV/£' 


33 


MEMOIR  NO.  1,  HUNTINGTON,   1911 


FIGURES  35  TO  41 


35 
36 

Same,  section  15. 
Same,  section  16. 

37 
38 

Same,  section  17. 
Same,  section  20. 

39 

Same,  section  22. 

40 

Same,  section  23. 

41 

Same,  section  24. 

1     Sympathetic  nerve. 
11     Jugular  lymph  sac. 
12    Jugular  lymph  sac,  thoracic  duct  approach 
16    Dorso-medial  somatic  venous  tributaries. 

22    Vagus. 
24    Thyrocervical  artery. 
25     Internal  jugular  vein. 
46    Left  superior  intercostal  vein. 

THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   2.1 


35 


, 


37 


38 


/ 


V 


•=•-•11 


** 


>•» 


24 
11 
12 


25 


39 


40 


24 


22 


•^m 

s     ^,     «  »» 


11 


12 


^ 


25 


41 


MEMOIR   NO.    1,    HUNTINOTON,    1911 


FIGURES  42  AND  43 

42  Same,  section  26. 

43  Transverse  section  through  left  side  of  lower  cervical  region  of  a  13.5  mm. 
cat  embryo  (series  189,  slide  VII,  section  10),  X  150. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

11  Jugular  lymph  sac. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

46    Left  superior  intercostal  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  26 


;.V  •  :<$||&p 

P?^5S^S?^C 

'     .   '    »      »'t  'J£tf 

1        ,*'.*           *««,*'                ,  *  '•  '  f       *      *  ^                                         M 

16 

»  •  k  .  •"  ,  "  •  '•  S&' 

/;Vv  '/••'»*  i*''*v-*.*v  V'  'x 

46 

,''••'.•  '  '.y      f 

"  ;  '\  *  ^.  'x^^  *  **"-.'''  *y^ 

11 

'  «*'*                      N***' 

"'-«     "»*NS-«  vf  ;  .f  ^-r*   ^  '+    c    *    *O^ 

'M 

•  ',  •'.  */                   Ji 

i^-L,*  "J%,  •'*  '*"*•.„'  :  *•  :  i. 

'X                                                       I 

1  •     ^»,                       y,t 

'-•^i^'?!' 

•         »»                   x  •*« 
1  1  •  •  •                 *<  "' 

v;r.^-y^  - 

*'Vv  VJV 

*  •  •  «*w       ^  *^' 

«5/>%\^i 

^va^j  • 

1 

'ta'V?*    •>       /^ 

^•'}     -' 

XK\  * 

'  >\- 

•   •>*^'4  » 

•'V^,   \A 

%«4 

99 

^^"4  •   • 

&im  %: 

* 

-•I/.     :'f     *\ 

»  •      * 

»>  f  >      •  1 

n  •  ii 
>V.-»v 

V^  V 

;  .•/^l 

Mttmft: 

42 


MEMOIR   NO.    1.   HUNTINGTON,    1911 


FIGURES  44  TO  49 


44 

Same,  section  11. 

45 

Same,  section  12. 

46 

Same,  section  13 

47 

Same,  section  14. 

48 

Same,  section  15. 

49 

Same,  section  16. 

1     Sympathetic  nerve. 

8    Oesophagus 

9     Trachea. 

11     Jugular  lymph  sac. 

12     Jugular  lymph  sac,  thoracic 

duct  approach 

16    Dorso-medial  somatic  venous  tributaries. 

17    Prevertebral  venous  plexus. 

22    Vagus. 

23    Left  carotid  artery. 

24    Thyrocervical  artery. 

25     Internal  jugular  vein. 

29    Jugulo-subclavian  trunk 

THE  SYSTEMIC    LYMPHATIC   VESSELS 


PLATE   27 


12 


17 


im 


16 

24 
11 

1 

22 

25 
23 


44 


25 


24 

11          12 


25 


25 


22 


24 


11 


25 


47 


48 


40IR    NO.    1,   HUNTINGTON,    1911 


FIGURES  50  TO  55 


50 

Same,  section  17. 

51 

Same,  section  18. 

52 

Same,  section  19. 

53 

Same,  section  20. 

54 

Same,  section  21. 

55 

Same,  section  22. 

1     Sympathetic  nerve. 

8    Oesophagus. 

11     Jugular  lymph  sac. 

12    Jugular  lymph  sac,  thoracic 

duct  approach. 

16    Dorso-medial  somatic  venous  tributaries. 

17     Prevertebral  venous  plexus. 

21     Thymus. 

22    Vagus. 

23     Left  carotid  artery. 

24    Thyrocervical  artery. 

25     Internal  jugular  vein. 

29     Jugulo-subclavian  trunk. 

THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  28 


29 


23 


24 


11 


25 


12 


22 


•  %>'  •-   *y  >  *  :^» >;».->•-. •<•. 
v    ">     .  v**-:'^-^  --^  *^  ';•  -5  V 

"•-^^>^,:>/5^»^^ 


24 


11 


25 


51 


52 


|M4     3£w 

fr*fl,lt  .">  v    ft  ..^*KiP    ^  fy 


12  y^*r  ^'•'•.^VY'*-'^''  '   J'<>T/S^' — *" — 

»    "  vi?^^(^  . 

gj^'^>       "^  *  - 
'  ^  -  j^l  ••      •'•  -.*  •  \'-'"* 

^^Ssi«v    -^Myp— 

22!^r^^e     ^^€^1^ 


24 


11 


25 


54 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURE  56 

56    Dissection  of  left  cervical  region  of  adult  cat,  showing  reduplication  of 
thoracic  duct  approach  of  left  jugular  lymph  sac  (Adult  No.  83). 

1  External  jugular  vein  and  lymphatic-.-. 

2  Common  jugular  vein. 

3  Jugular  lymph  sac. 
5  Subclavian  vein. 

9  Thyrocervical  artery. 

11  Vertebral  vein. 

13  Left  subclavian  artery. 

18  Jugular  approach  and  tap. 

19  Subclavian  approach  and  tap. 

20  Innominate  artery. 

24  Vena  cava  superior. 

25  Left  carotid  artery. 

26  Aorta, 


THE  SYSTEMIC   LYMPHATIC  VESSELS 


PLATE  29 


18 


20 


26 


13 


MfiMOIR  NO.   1,   HUNTING-TON,  1911 


FIGURES  57  AND  58 

57  Transverse  section  through  left  lower  cervical  region  of  a  14  mm.  cat  embryo 
(series  122,  slide  IX,  section  21) ,  X  150. 

58  Same,  section  28. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 
16  Dorso-medial  somatic  venous  tributaries. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

26  Common  jugular  vein. 
29  Jugulo-subclavian  trunk. 


PLATE  30 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


1%  •„'.**,.  I..."    >  •.**'*•  A 

ifeull 


FIGURES  59,  60  AND  61 

59  Same,  slide  X,  section  7. 

60  Same,  section  9. 

61  Same,  section  12. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 
26  Common  jugular  vein. 

30  Sixth  spinal  nerve. 

31  Primitive  ulnar  veno-lymphatic. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  31 


22 
23 


24 


12 


26 


t  I  Ti  i'  *i  <"    '    i  AJT   •,•'•&'    •*.    '  w  •••  ..  ~*  ^»*.'T»»?^% ^on* 

SI^^^^IFii     ^^':  0y^^ 


60 


MEMOIR  NO.    1,   HUNTINGTON,    1911 


FIGURES  62  AND  63 

62  Same,  section  13. 

63  Transverse  section  of  left  lower  cervical  region  in  a  13  mm.  cat  embryo 
(series  92,  slide  X,  section  27),  X  225. 

1  Sympathetic  nerve. 

8  Oesophagus. 

11  Jugular  lymph  sac. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 
16  Dorso-medial  somatic  venous  tributaries. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

26  Common  jugular  vein. 

29  Jugulo-subclavian  trunk. 

30  Sixth  spinal  nerve. 

31  Primitive  ulnar  veno-lymphatic. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  32 


'          - : 


!,,  9&        ifr.X 


22 


0.,'i0^-'.-wp  ,       , 

fW.S^lSr  -"V-J^ 

&\  V  ^  •- ;  ;  >Y    *  *  «jt  .^^ 

*.J'';V-'  -.,^f        ^fe-3 
lr*^A>'w   v;J-  4^r^ 


•  *  •     fTr*««^»^ 

%«  Jt  4-->V. 

ffi  ^e  ••*      *355jJU* 

**     «.         ^-4Cl       Z'&X' 

,    .V  ^,/-'  *^* 


r » » f '  J'*/, 

P^;S\^>< 

IB^sS?! 

Wtt$*<f  &Jr%,  ±3 

»Jl. 


->?' 


IT-'     ;  i*  •#''v-.- 

.  ;-??"r.  ./*^     t^        ft^'"*   ""* 


13 


29 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  64,  65  AND  66 

64  Same,  section  31. 

65  Same,  section  32. 

66  Same,  section  33. 

1  Sympathetic  nerve. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 
22  Vagus. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

29     Jugulo-subclavian  trunk. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  33 


29 


64 


29 


14 


24 


13 


*29 


66 


MEMOIR  NO.   1,   HUNTINGTON,   1911 


FIGURES  67,  68  AND  69 

67  Same,  section  35. 

68  Same,  section  36. 

69  Same,  section  38. 

1  Sympathetic  nerve. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

29    Jugulo-subclavian  trunk. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  34 


JEMOIK   NO.    1,    HUNTINGTON,    1911 


FIGURES  70,  71  AND  72 

70  Same,  slide  IX,  section  2. 

71  Same,  slide  IX,  section  5. 

72  Same,  slide  IX,  section  6. 

1  Sympathetic  nerve. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

22  Vagus. 

24  Thyrocervical  artery. 

26  Common  jugular  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  35 


*?^imT 


STf     » 

aTMskJ-JfJ 

%*>,«* 


24 


14 


26 


71 


$  J^W*  3r^>  ** 


26 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  73,  74  AND  75 

73  Same,  slide  IX,  section    9. 

74  Same,  slide  IX,  section  10. 

75  Same,  slide  IX,  section  11. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

22  Vagus. 

24  Thyrocervical  artery. 

26  Common  jugular  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  36 


MEMOIR   NO.    1.   HUNTINGTON,    1911 


FIGURES  76,  77  AND  78 

76  Same,  slide  IX,  section  12. 

77  Same,  slide  IX,  section  13. 

78  Same,  slide  IX,  section  14. 

1    Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus. 
22  Vagus. 

24    Thyrocervical  artery. 
26    Common  jugular  vein. 


PLATE  37 


'  *  <  ^k.^r*'  *    .  •*  *  * 

-•*  •  r-V.-,vJ^  \^v» 

J^fln.        MI    *tfl^»«*9fe^.       ,_»""^i>    *i 


26 


MEMOIR   NO.   1,   HCNTINGTON,   1911 


EXPLANATION   OF    FIGURE    79 

79    Transverse  section  of  left  lower  cervical  region  in  a  15  mm.  cat  embryo 
(series  245,  slide  XI,  section  24),  X  225. 

1  Sympathetic  nerve. 

8  Oesophagus. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 
26  Common  jugular  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  38 


79 


MEMOIR    NO.   1,    HUNTINGTON,   1911 


FIGURES  80,  81  AND  82 

80  Same,  section  25. 

81  Same,  section  26. 

82  Same,  section  27. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 
26  Common  jugular  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  39 


*•   *  ^hstF^w^**  -  W««JSi^  ^»Ift      A* 

^•^r^Jjf^yif^sfi^fo.  "H^  /V 


26 


80 


•      .  ..v:v--*«Sfr,Y  .r*J    fjS 

x  **•;  -vr    .;/;?-& 

•  ••  .>'>:v:^ .•••••••»  /,"; 


81 


12 


16 


24 


-i 


MKMOIR   XO.    1,   HUNTINGTON,   1911 


FIGURES  83  AND  84 

83  Transverse  section  of  left  lower  cervical  region  in  a  17  mm.  cat  embryo 
(series  142,  slide  X,  section  13),  X  225. 

84  Same,  section  16. 

1  Sympathetic  nerve. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

21  Thymus. 

22  Vagus. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

29     Jugulo-subclavian  trunk. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE        40 


29 


2J 


MEMOIR   NO.   1,   HUNTINCiTON,    1911 


FIGURES  85  AND  86 

85  Same,  section  18. 

86  Same,  section  20. 

1  Sympathetic  nerve. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 

21  Thymus. 

22  Vagus. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 

29    Jugulo-subclavian  trunk. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   41 


21 


13 


MKMOIlt    NO.    1,    HUNTINGTON,   1911 


FIGURES  87  AND  88 

87  Same,  section  22. 

88  Same,  section  24. 

1  Sympathetic  nerve. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 

14  Jugular  lymph  sac,  subclavian  approach. 
16  Dorso-medial  somatic  venous  tributaries. 

21  Thymus. 

22  Vagus. 

24  Thyrocervical  artery. 

25  Internal  jugular  lymphatics. 
29     Jugulo-subclavian  trunk. 


THE  SYSTEMIC   LYMPHATIC  VESSELS 


PLATE  42 


24 


14 


29 


13 


24 


21 


MKMOIH    NO.    1.    HUNTINCJTON,    Iflll 


DEVELOPMENT  OF  THE  THORACIC  DUCT  83 


2.  THE  PREAZYGOS  SEGMENT 

This  portion  of  the  thoracic  duct  develops,  again  by  confluence 
of  numerous  extraintimal  perivenous  anlages,  in  the  cephalic 
and  lateral  mediastinal  space,  between  the  termination  of  the 
thoracic  duct  approach  of  the  jugular  sac  and  the  level  of  the 
intersection  of  the  left  duct  with  the  aortic  arch.  Its  ontogenesis 
offers  the  most  striking  and  definite  evidence  of  the  development 
of  the  systemic  lymphatic  channels  in  this  mammalian  embryo 
as  the  result  of  the  confluence  of  a  large  number  of  originally 
separate  and  independent  "extra-intimal"  or  "  perivenous" 
mesodermal  spaces,  following  and  enveloping  the  early  embryonal 
veins,  or  completely  surrounding  them,  and  finally  entirely  replac- 
ing them.  The  spaces  which  I  am  describing  as  the  anlages  of 
the  systemic  lymphatic  channels  in  the  mammalian  embryo  under 
consideration  (Felis  domesticd)  are  surely  easy  enough  to  see.  If 
they  are  followed  in  successive  stages  they  fully  and  completely 
reveal  the  histogenesis  of  the  systemic  lymphatic  vessels  in  this 
mammalian  form,  and  conclusively  establish  the  relation  of  the 
first  mammalian  lymphatic  anlages  to  the  embryonic  veins,  which 
they  are  destined  to  replace,  as  previously  outlined  in  the  prelim- 
inary publications  quoted  (1,  2,  21,  22).  The  structures  which 
form  the  first  anlages  of  the  systemic  lymphatic  channels  in 
the  embryo  of  the  cat  cannot  be  injected,  because  at  the  time 
of  their  first  definite  appearance  they  represent  the  still  disjointed 
links  of  a  chain  which  is  only  subsequently  to  be  assembled  into 
a  continuous  whole.  It  is  possible  to  inject  in  earlier  periods 
the  veins  which  are  later  replaced  by  these  extraintimal  lymphat- 
ics, and  it  is  possible  to  inject  in  later  stages  the  lymphatics 
when  they  have  united  into  a  connected  system  of  channels. 
But  in  either  case  injection  methods  merely  prove  topographi- 


84         DEVELOPMENT    OF   THE    SYSTEMIC    LYMPHATIC  VESSELS 

cal  conditions  for  any  given  stage.  They  afford  absolutely  no 
proof  of  the  histogenetic  origin  of  vascular  structure.  The  mere 
fact  that  a  lymphatic  plexus  occupies  topographically  the  place 
of  an  antecedent  venous  plexus  is  absolutely  no  proof  of  the 
histogenetic  identity  of  the  channel  system  involved.  However, 
to  return  to  the  matter  in  hand,  while  the  region  under  discussion 
serves  no  better  than  any  other  part  of  the  embryo  for  this  pur- 
pose, it  fully  and  completely  illustrates  the  relative  condition  of 
embryonic  veins  and  the  replacing  extraintimal  lymphatics  in  the 
genesis  of  the  adult  systemic  lymphatic  channels. 

The  ontogenetic  history  of  the  preazygos  segment  of  the  thoracic 
duct  must  be  considered  in  reference  to  three  regions: 

A.  The    development    of    a    broncho-mediastinal    or    ventral 
mediastinal  lymphatic  channel,  draining  the  ventral  and  lateral 
mediastinal  areas,  cephalad  of  the  pericardium,  and  including 
the  lymphatic  return  from  the  thymic,  tracheal,  bronchial,  and 
oesophageal  regions. 

B.  The  development  of  the  proximal  portion  of  the  thoracic 
duct  proper,  between  the  termination  of  the  thoracic  duct  ap- 
proach of  the  jugular  lymph  sac,  and  the  beginning  of  the  azygos 
segment  of  the  thoracic  ducts,  caudal  to  the  level  of  the  aortic 
arch. 

C.  The  junction  of  these  two  independently  formed  lymphatic 
trunks  with  each  other  and  with  the  thoracic  duct  approach  of 
the  jugular  lymph  sac. 

Adult  Conditions 

Before  taking  up  the  embryological  consideration  of  the  develop- 
ment of  these  channels  and  the  establishment  of  their  subsequent 
connections,  it  seems  advisable,  on  account  of  the  complicated 
topographical  relations,  to  establish  these  clearly  by  reference 
to  a  small  selected  series  of  adult  animals  with  successful  injection 
of  the  lymphatic  structures  concerned.  This  becomes  all  the 
more  necessary  because  the  adult  variations  observed  in  the 
arrangement  of  the  lymphatics  of  this  region  have  an  important 


DEVELOPMENT  OF  THE  THORACIC  DUCT  85 

bearing  on  the  observed  embryological  conditions.  An  under- 
standing of  the  former  is  necessary  for  the  correct  interpretation 
of  the  latter,  and  vice  versa.  Hence,  while  the  details  of  the 
adult  anatomy  of  the  cat's  lymphatic  system  in  its  relation  to 
the  development  are  reserved  for  Part  V  of  the  second  publica- 
tion of  this  series,  a  limited  number  of  adult  illustrations  are  here 
introduced  in  order  to  prepare  the  ground  for  the  consideration 
of  the  ontogenesis  of  the  broncho-mediastinal  trunk  and  of  the 
preazygos  segment  of  the  thoracic  duct. 

In  a  certain  proportion  of  adults  the  ventral  or  broncho- 
mediastinal  trunk  has  no  direct  connection  with  the  preazygos 
segment  of  the  thoracic  duct,  but  drains  solely  cephalad  into  a 
ventral  prolongation  from  the  subclavian  approach  of  the  jugular 
sac,  which  process  also  receives  the  main  lymph  vessels  from  the 
axilla  and  the  forelimb. 

Figs.  92  and  93  (adults,  nos.  67  and  13)  give  good  illustrations 
of  this  condition. 

In  many  other  adults,  however,  the  left  ventral  or  broncho- 
mediastinal  trunk  is  connected  caudally,  with  or  without  the 
interposition  of  one  or  more  lymph  nodes  common  to  both,  with 
the  preazygos  segment  of  the  thoracic  duct.  This  junction  com- 
monly occurs  about  at  the  level  at  which  the  innominate  artery 
divides.  The  cephalic  extremity  of  the  main  broncho-mediastinal 
trunk  then  usually  still  drains  into  the  jugular  lymph  sac  by 
establishing  a  connection  with  the  ventral  prolongation  which 
the  subclavian  approach  of  the  sac  sends  caudad  over  the  ventral 
aspect  of  the  jugulo-subclavian  confluence.  This  process  also 
receives  the  main  lymphatic  trunks  from  the  anterior  extremity 
and  from  the  axillary  area  of  the  thoracic  wall.  Occasionally  the 
cephalic  end  of  the  broncho-mediastinal  trunk  also  connects  with 
the  similar  ventral  prolongation  which  the  jugular  approach  of 
the  lymph  sac  sends  down  over  the  ventral  aspect  of  the  common 
jugular  angle  of  confluence. 

The  broncho-mediastinal  trunk  is  therefore  usually  represented 

vby  a  ventral  lymph  channel  of  some  size,  whose  caudal  extremity 

joins  the  preazygos  segment  of  the  thoracic  duct,  while  its  cephalic 

extremity  empties,  in  common  with  other  axial  and  appendicular 


86         DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

lymph  paths,  into  the  caudal  end  of  the  jugular  sac,  usually  into 
the  ventral  process  of  the  subclavian  approach  caudal  to  the 
jugulo-subclavian  lymphatico- venous  tap.  In  this  course  the 
broncho-mediastinal  trunk  receives  afferents  from  the  medias- 
tinal  structures.  Fig.  94  shows  this  general  arrangement  on  the 
left  side  in  a  typical  adult  (No.  56),  in  which  the  left  jugular 
lymph  sac  connects  with  the  veins  only  through  the  single  jugulo- 
subclavian  tap.  A  double  ventral  process  from  the  subclavian 
approach  effects  the  cephalic  connection  of  the  broncho-medias- 
tinal trunk  with  the  jugular  sac,  while  caudally  two  lymph  vessels 
unite  it  to  the  preazygos  segment  of  the  thoracic  duct. 

It  is  evident  in  following  the  thoracic  duct  caudo-cephalad 
that  this  arrangement  enables  the  flow  of  lymph  in  the  main 
canal  to  take,  near  the  level  of  the  innominate  bifurcation,  one 
of  two  equally  available  pathways  in  order  to  reach  the  jugular 
sac  and  through  it  enter  the  venous  stream: 

a.  It  may,  in  large  part  or  entirely,  continue  cephalad  in  the 
dorsal  channel  of  the  preazygos  segment  of  the  thoracic  duct 
proper,  or 

6.  It  may  ascend  in  the  channel  of  the  broncho-mediastinal 
trunk,  and  empty  into  the  venous  system  through  the  ventral 
prolongation  of  the  subclavian  approach  of  the  jugular  lymph 
sac. 

This  arrangement,  which  furnishes  the  keynote  for  the  main 
variations  of  the  thoracic  duct  in  this  region,  and  for  the  interpre- 
tation of  certain  important  embryological  stages,  is  well  illustrated 
by  the  dissection  of  the  left  side  of  neck  and  thorax  in  the  adult 
cat  shown  in  fig.  95  (adult,  no.  22).  The  azygos  segment  of  the 
thoracic  duct  is  seen  caudad  of  the  level  of  azygos  arch  (21)  as  a 
plexiform  channel  whose  meshes  are  perforated  by  the  inter- 
costal arteries.  Cephalad  of  the  azygos  arch  the  preazygos  seg- 
ment of  the  thoracic  duct  continues  as  an  undivided  canal  of 
larger  caliber  to  the  level  of  division  of  the  innominate  artery 
(20).  At  this  point  the  broncho-mediastinal  trunk  (8)  diverges 
from  the  main  canal  and  ascends  ventral  to  the  left  subclavian 
artery,  receiving  tributaries  from  the  ventral  mediastinal  nodes. 
It  meets  the  subclavian  lymphatic  and  a  large  ventral  mediastinal 


DEVELOPMENT  OF  THE  THORACIC  DUCT  87 

trunk  accompanying  the  internal  mammary  vessels  (7)  in  front  of 
the  jugulo-subclavian  angle  in  a  plexiform  junction,  which  empties 
into  a  ventral  process  prolonged  down  from  both  the  jugular  (18) 
and  subclavian  (19)  approaches  of  the  jugular  lymph  sac. 

The  preazygos  segment  of  the  thoracic  duct,  cephalad  of  its 
connection  with  the  broncho-mediastinal  trunk,  takes  the  usual 
course  upward  under  cover  of  the  subclavian  artery  and  behind 
the  vertebral  vein  (11)  and  opens  into  the  dorsal  aspect  of  the 
jugular  sac  a  little  in  front  of  the  common  jugular  tap. 

The  jugular  lymph  sac  is  well  developed  in  its  ventral  division 
and  opens  into  the  venous  system  at  the  two  typical  points,  viz., 
both  at  the  common  jugular  and  jugulo-subclavian  taps.  It 
receives  the  internal  and  external  jugular  and  the  cephalic  lym- 
phatics in  the  usual  way.  The  subclavian  vein  (5)  is  divided 
close  to  the  jugulo-subclavian  confluence  and  turned  forward  to 
expose  the  vertebral  vein  and  the  duct. 

The  individual  affords  a  good  example  of  the  full  development 
of  the  normal  preazygos  segment  of  the  thoracic  duct  in  combina- 
tion with  a  well  marked  broncho-mediastinal  trunk  and  plexus. 
The  former  is  still  the  main  lymphatic  channel,  although  the 
broncho-mediastinal  vessel  is  fully  developed  and  capable  of 
draining  the  mediastinal  lymphatics  either  cephalad  into  the 
lymph  sac  or  caudad  into  the  thoracic  duct. 

Fig.  96  (adult,  no.  29)  shows  an  instance  in  which  the  preazy- 
gos segment  of  the  thoracic  duct  (12)  and  the  broncho-mediastinal 
trunk  (8)  are  of  nearly  equal  size,  the  former  receiving  the  inter- 
nal mammary  (6)  and  inferior  thyroid  (4)  lymphatics  and  drain- 
ing into  the  jugular  sac  through  the  ventral  prolongation  of  its 
subclavian  approach.  The  preparation  shows  well  the  main 
relations  of  the  lymphatic  complex  to  the  vertical  portion  of  the 
left  subclavian  artery  (13)  and  its  branches,  with  the  broncho- 
mediastinal  trunk  (8)  lying  ventral  to  the  artery,  while  the  tho- 
racic duct  (2)  ascends  dorsal  to  the  same,  and  further  passes  be- 
neath the  vertebral  vessels  (11)  and  the  thyro-cervical  artery  (9)  in 
order  to  reach  its  connection  with  the  lymph  sac.  The  latter  has 
in  this  instance  a  single  tap  into  the  veins  through  the  subclavian 
approach  at  the  jugulo-subclavian  angle.  The  subclavian  vein  (5) 


88        DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

has  again  been  cut  short  and  turned  mesad  to  expose  the  deeper 
structures. 

The  azygos  segment  of  the  thoracic  duct  (16)  shows  the  same 
plexiform  character  and  relation  to  the  perforating  intercostal 
arteries  as  in  the  preceding  dissection  (fig.  95). 

Fig.  97  (adult  no.  131)  shows  an  instance  in  which  the  main 
thoracic  duct  turns  ventrad  into  the  broncho-mediastinal  trunk, 
while  a  small  channel  follows  the  usual  dorsal  course  of  the  normal 
duct. 

The  left  jugular  lymph  sac  has  only  a  single  tap  into  the  venous 
system  at  the  jugulo-subclavian  angle. 

The  sac  receives  at  its  cephalic  end  two  lymphatic  trunks  paral- 
leling the  internal  jugular  vein  (17),  which  is  larger  than  usual, 
and  the  combined  trunk  formed  by  the  external  jugular  and 
cephalic  lymphatics. 

The  dorsal  half  of  the  thyro-cervical  periarterial  ring  is  smaller 
than  the  ventral,  but  the  foramen  is  complete. 

The  jugulo-subclavian  approach  and  tap  is  formed  by  a  large 
process  of  the  sac  which  sends  a  ventral  prolongation  over  the 
jugulo-subclavian  angle.  This  receives  laterally  the  subciavian 
lymphatic,  ascending  along  the  subciavian  vein  (5),  and  from 
below  the  broncho-mediastinal  trunk  (8),  which  represents  the 
main  cephalic  continuation  of  the  thoracic  duct.  The  duct  at  the 
aortic  arch  level  (26)  splits  into  a  smaller  dorsal  (12)  and  larger 
ventral  division  (8).  The  former  ascends  behind  the  vertical 
part  of  the  subciavian  artery,  crosses  behind  the  vertebral  vein, 
and  turning  ventro-caudad  around  the  lateral  aspect  of  the  thyro- 
cervical  artery  (9),  enters  the  dorsal  aspect  of  the  jugular  lymph 
sac,  just  in  front  of  the  jugulo-subclavian  tap.  This  smaller 
dorsal  division  represents  the  usual  preazygos  portion  of  the 
thoracic  duct  of  the  adult. 

The  second  larger  division  of  the  duct  takes  the  path  of  the 
broncho-mediastinal  channel  (8).  It  ascends  first  on  the  outer 
side  and  then  in  front  of  the  subciavian  artery,  subdivides  into 
two  branches,  which  reunite  and  receive  a  small  lymphatic  from 
the  left  innominate  plexus.  The  upper  end  of  the  duct  crosses 
in. front  of  the  junction  of  the  vertical  and  arched  portions  of  the 


DEVELOPMENT  OF  THE  THORACIC  DUCT  89 

subclavian  artery  and  in  front  of  the  subclavian  vein  to  terminate, 
in  common  with  the  subclavian  lymphatic,  in  the  ventral  process 
of  the  subclavian  approach  of  the  lymph  sac. 

More  rarely  the  broncho-mediastinal  channel  forms  the  only 
terminal  path  of  the  thoracic  duct.  In  these  instances  the 
preaortic  segment  of  the  thoracic  duct  abandons  its  normal  dorsal 
position  and  turns  ventrad  into  the  path  of  the  broncho-medias- 
tinal channel.  Thus  in  fig.  98  (adult,  no.  168),  in  which  the 
common  jugular  tap  (18)  is  the  only  lymphatico-venous  con- 
nection of  the  left  jugular  lymph  sac,  the  ventral  process  of  the 
jugular  approach  is  free  and  prolonged  caudo-ventrad  over  the 
jugulo-subclavian  angle  as  a  large  trunk  which  receives  the  entire 
drainage  of  the  thoracic  duct.  'The  latter  (8),  after  passing  the 
aortic  arch,  swings  ventrad  of  the  subclavian  artery  into  the 
pathway  of  the  normal  broncho-mediastinal  trunk  and  ascends 
to  meet  the  ventral  prolongation  of  the  jugular  approach  of  the 
lymph  sac. 

It  thus  becomes  apparent  that  in  dealing  with  the  ontogenesis 
of  the  cephalic  portion  of  the  cat's  thoracic  duct  it  is  necessary 
to  reckon  with  the  ventral  mediastinal  and  broncho-mediastinal 
channels  as  well  as  with  the  preazygos  segment  of  the  thoracic 
duct  proper,  since  the  former,  as  just  seen,  may  take  over,  par- 
tially or  entirely,  the  drainage  of  the  duct  into  the  jugular  lymph 
sac. 

A  composite  schema  of  the  adult  preazygos  portion  of  the  tho- 
racic duct  in  relation  to  the  broncho-mediastinal  and  ventral 
mediastinal  trunks  is  given  in  fig.  99  based  on  the  individual  con- 
ditions encountered  in  the  adult  series  examined.  The  plan  rep- 
resents every  recorded  development  of  the  lymphatic  pathways 
in  this  region,  but  is  rarely  seen  in  its  full  development  in  the 
adult  (cf.  adult,  no.  29,  fig.  96).  Usually  one  or  more  of  these  po- 
tential segments  and  connections  default  and  thus  a  great  variety 
of  distinct  adult  conditions  is  produced.  These  lymphatic  path- 
ways are,  however,  all  present  in  the  embryo  and  account  for 
the  observed  adult  variants. 


PART  II,  PLATES 

FIGURES  92  TO  99 


FIGURES  92  AND  93 

92  Dissection  of  the  veins  and  lymphatics  at  the  root  of  1  he  nrck  in  an  adult  cat, 
(No.  67). 

93  Same.,  No.  13. 

(Figs.  92,  93,  and  94  are  republished  from  Huntington  and  McClure's  "  Anatomy 
and  Development  of  the  Jugular  Lymph  Sacs  in  the  Domestic  Cat,"  Am.  Jour. 
Anat.,  Vol.  X,  No.  2.) 


TIIK   SYSTEMIC   LYMPHATIC   VESSELS 


INT.  JUGULAR   VHN 


LEFT    EXT.  JUGULAR    VEIN 


THYRO-CERVIC 


COMMON    JUGULA 
COMMON    JUGU 


SUBCLAVIAN  APPROAC 


INNOMINATE    VE 


92 

INT    JUGULAR   VEIN 


RIGHT   EXT.  JUG.  V 


THVRO-CERVICAL   A 

JUGULO-CEPHALIC    TRUN 


JUGULO   SUBCLAVIAN  TAp 
INNOMINATE   VEIN 


HYRO-CERVICAL   A 

UGULAR    TAP 
AN   APPROACH 
SUBCLAVIAN    V. 


THORACIC   DUCT 


LEFT   EXT.  JUG    V 


EPHALIC    VEIN 


THYRO-CERVICAL   A. 
OMMON    JUGULAR   TAP 


—  SUBCLAVIAN    V. 
COMMON    JUGULAR    V. 


—  THORACIC  DUCT 


93 


MEMOIR   NO.    1,   HUNTINGTON,    Iflll 


FIGURE  94 
94    Same,  No.  56. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  45 


INT.  JUGULAR   VEIN 


LEFT  EXT.  JUG.  V. 


RIGHT  EXT.  JUG.  V 


CEPHALIC   VEIN 
\ 


THYRO-CERV1CAL   A 

JUGULO- CEPHALIC    TRUN 
COMMON   JUGULAR   V 


JUGULO 
,—mm  /       SUBCLAVIAN 

SUBCLAVIAN    V 


SUBCLAVIAN 
APPROACH 

INNOMINATE   VEIN 


CEPHALIC    VEIN 


THYRO-CERVICAL   A. 

JUGULO-CEPHALIC    TRUNK 
SUBCLAVIAN   APPROACH 


SUBCLAVIAN    V 


JUGULO-SUBCLAVIAN   TAP 


INNOMINATE   VEIN 


94 


MEMOIR  NO.    1,   HUNTINGTOK,    1911 


FIGURE  {)•> 

95     Dissection  of  main  lymphatic  vessels  of  neck  and  thorax  in   an   adult    cat 

(No.  22). 

1  External  jugular  vein  and  lymphatics. 

5  Subclavian  vein. 

7  Internal  mammary  artery  and  lymphatics. 

S  Broncho-mediastinal  or  ventral  mediastinal  lymphatic  trunk. 

10  Cephalic  vein  and  lymphatics. 

11  Vertebral  vein. 

12  Thoracic  duct,  preazygos  segment. 
15  Oesophagus. 

17  Internal  jugular  vein  and  lymphatics. 

18  Jugular  approach  and  tap. 

19  Subclavian  approach  and  tap. 

20  Innominate  artery. 

21  Azygos  vein. 


TIIK   SYSTEMIC  LYMPHATIC   VESSELS 


PLATE*  46 


21 


17 


12 


—  15 


MEMOIK   NO.    1,    HUNTINGTON,    1911 


FIGURE  90 

96    Dissection  of  main  lymphatic  vessels  of  neck  and  thorax  in  an  adult  cat 

(No.  29). 

1  External  jugular  vein  and  lymphatics. 

2  Common  jugular  vein. 

3  Jugular  lymph  sac. 

4  Inferior  thyroid  lymphatics. 

5  Subclavian  vein. 

6  Internal  mammary  lymphatics. 

7  Internal  mammary  artery. 

8  Broncho-mediastinal  or  ventral  rnediastinal  lymphatic  trunk 

9  Thyrocervical  artery. 

10  Cephalic  vein  and  lymphatics. 

11  Vertebral  vein. 

12  Thoracic  duct,  preazygos  segment. 

13  Left  subclavian  artery. 

14  Junction  of  preazygos  and  azygos  segments  of  thoracic  duct. 

15  Oesophagus. 

16  Azygos  segment  of  thoracic  duct. 


THE  .SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  47 


MEMOIR   NO.   1,   HONTINGTON,   1911 


FIGURE  97 

97     Dissection  of  main  lymphatic  vessels  of  neck  and   thorax  in   an   adult  cat 
(No.  131). 

1  External  jugular  vein  and  lymphatics. 

2  Common  jugular  vein. 
5  Subclavian  vein. 

7  Internal  mammary  artery. 

8  Broncho-mediastinal  or  ventral  mediastinal  lymphatic  trunk. 

9  Thyrocervical  artery. 

12  Thoracic  duct,  preazygos  segment. 

13  Left  subclavian  artery. 

15  Oesophagus. 

16  Azygos  segment  of  thoracic  duct. 

17  Internal  jugular  vein  and  lymphatics. 
20  Innominate  artery. 

23  Innominate  vein. 

26  Aorta. 

27  Vagus  nerve. 

28  Inferior  thyroid  vein. 

29  Jugulo-cephalic  venous  trunk. 


THE   SYSTEMIC  LYMPHATIC   VESSELS 


PLATE  48 


97 


MKMOIH   NO.   1,    HUNTINGTON,    1911 


FIGURE  <)S 

98     Dissection  of  left  jugular  lymph  sac  and  thoracic  duct  in  an  adult  cat  (No 

168). 

2  Common  jugular  vein. 

5  Subclavian  vein. 

8  Broncho-mediastinal  or  ventral  mediastinal  lymphatic  trunk. 

9  Thyro-cervical  artery. 
13  Left  subclavian  artery. 
15  Oesophagus. 

17  Internal  jugular  vein  and  lymphatics. 

18  Jugular  approach  and  tap. 

21  Azygos  vein. 

22  Trachea. 

23  Innominate  vein, 

24  Vena  cava  superior 

25  Left  carotid  artery. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  49 


22 


17 


98 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FKHIRE  09 

09     Schema  showing  composite  picture  of  left  jugular  lymph  sac,  broncho  me 
diastinal  trunk  and  preazygos  segment  of  thoracic  duct. 

1  External  jugular  vein  and  lymphatics. 

3  Jugular  lymph  sac. 

5  Subclavian  vein. 

6  Internal  mammary  lymphatics. 

8  J3roncho-mediastinal  or  ventral  mediastinal  lymphatic  trunk. 

9  Thyro-cervical  artery. 

10  Cephalic  vein  and  lymphatics. 

11  Vertebral  vein. 

12  Thoracic  duct,  preazygos  segment. 

13  Left  subclavian  artery. 

16  Azygos  segment  of  thoracic  duct. 

17  Internal  jugular  vein  and  lymphatics. 

18  Jugular  approach  and  tap. 

19  Subclavian  approach  and  tap. 

20  Innominate  artery. 

23  Innominate  vein. 

24  Vena  cava  superior. 
2i3  Left  carotid  artery. 
26  Aorta. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   5(1 


17 


10 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


DEVELOPMENT  OF  THE  THORACIC  DUCT  91 

The  Development  of  the  Broncho-Mediastinal  Trunk  and  of  the 
Preazygos  Segment  of  the  Thoracic  Duct 

The  area  in  which  the  development  of  the  broncho-mediastinal 
and  preazygos  segments  of  the  thoracic  duct  occurs  is  shown  in 
fig.  100,  which  gives  a  topographical  view  of  a  transection  of  the 
upper  thoracic  region  in  a  12  mm.  embryo  (series  78,  slide  IX, 
section  5,  X  50). 

The  section  includes  the  entire  coelom  ventrally,  and  the 
structures  between  it  and  the  notochord  dorsally.  The  right  (3) 
and  left  (6)  precaval  veins  occupy  the  lateral  limits  of  the  dorsal 
region.  In  the  interval  between  them  are  seen  the  oesophagus 
(8),  the  trachea  (9),  the  vagi  (22)  and  the  dorsal  aortic  arches 
(7).  Dorsal  to  the  main  veins  on  each  side  are  the  strands  of  the 
brachial  plexus  (not  labelled  in  the  figure),  and  dorsal  to  the 
nerves  is  the  primitive  ulnar  veno-lymphatic  (31).  Further 
mesad  follow  the  subclavian  arteries  (33),  the  entrance  of  the 
dor  so-medial  venous  tributaries  (16)  into  the  main  veins,  and  the 
sympathetic  strands  (1).  The  letter  Y  in  the  figure,  between 
the  notochord  and  the  dorsal  mediastinal  structures  named, 
indicates  the  center  of  the  area  in  which  the  development  of  the 
preazygos  segment  of  the  thoracic  duct  will  proceed  in  the  suc- 
ceeding stages. 

The  ventral  portion  of  the  field  contains  the  coelom,  with  right 
(48)  and  left  (49)  auricles,  right  ventricle  (50),  ascending  aorta  (7) 
and  ascending  trunk  of  main  pulmonary  artery  (10).  Dorsal  to 
this  are  seen  the  cross-sections  of  the  right  and  left  pulmonary 
arteries  (10)  descending  to  the  lungs.  Between  them  ventrally, 
and  trachea  (9),  aortae  (7),  vagi  (22)  and  praecaval  veins  (3,  6) 
dorsally,  is  the  area  marked  by  the  letter  X,  in  which  the  develop- 
ment of  the  broncho-mediastinal  trunk  will  proceed. 

A .  The  development  of  the  broncho-mediastinal  or  ventral  medias- 
tinal lymphatic  channels,  which  drain  subsequently  caudo-sinistrad 
into  the  left  thoracic  duct,  or  cephalo-sinistrad  into  the  subclavian 
approach  of  the  jugular  lymph  sac,  or  into  both. 

In  the  earlier  stages  (embryos  of  11-14  mm.),  an  extensive 
ventral  venous  capillary  network  develops  between  the  main 


92        DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC    VESSELS 

venous  trunks  of  the  right  and  left  sides,  involving  the  distal  part 
of  the  internal  jugular,  the  common  jugular  and  the  innomi- 
nate veins. 

Out  of  this  general  antecedent  sinistro-dextral  capillary  reticu- 
lum  the  definite  retro-  or  suprathymic  innominate  anastomosis 
develops  subsequently  in  normal  individuals,  but  in  the  earlier 
stages  this  plexus  extends  both  ventral  and  dorsal  to  the  thymus 
anlage. 

The  venous  network  develops,  in  addition  to  the  prevertebral 
and  dorsal  somatic  components,  chiefly  on  the  lateral  aspect  of  the 
oesophagus,  in  the  peri-tracheal  area,  and  around  the  thymus  and 
the  common  carotid  artery.  It  trends  cephalo-laterad  towards 
the  main  venous  lino  (jugulo-innominate),  into  whose  mesal  sur- 
face the  terminals  of  the  plexus  discharge. 

In  so  doing  they  encounter,  and  partially  surround,  the  sym- 
pathetic and  vagus  nerves,  and  the  thymus  body.  Consequently 
the  terminal  branches  of  this  ventral  mediastinal  plexus  enter 
the  main  vein  both  ventral  and  dorsal  to  these  three  structures 
and  through  the  intervals  between  them.  Thus  the  composite 
plan  of  this  venous  area  appears  as  shown  in  the  schematic  fig. 
101,  which  represents  the  combination  of  a  number  of  transverse 
sections  of  the  anterior  thoracic  region. 

The  terminal  connections  of  the  ventral  mediastinal  plexus 
may  be  grouped  in  reference  to  their  derivation  and  their  relation 
to  adjacent  fields  of  venous  drainage  into  the  following  five  sets, 
(fig.  101): 

1.  Dorso-medial  somatic  tributaries  of  internal  and  common 
jugular  and  of  innominate  veins  (fig.  101,  16}  entering  the  main 
venous  channel  dorsal  to  the  sympathetic  nerve,  and  frequently 
combined  with 

2.  Terminal  of  prevertebral  venous  plexus  anterior  to  azygos 
veins  (fig.  101,  17). 

3.  Terminal   of  peritracheal  plexus  passing   laterad  between 
sympathetic  (1)  and  vagus  (22)  nerves  (fig.  101,  18). 

4.  Ventral    mediastinal    branch,    draining,    as    "  suprathymic 
plexus,"  the  area  between  the  thymus  (21),  carotid  (23)  and 
vagus  (22).     This  is  the  line  of  the  future  typical  permanent  left 
innominate  anastomosis  dorsal  to  the  thymus  (fig.  101,  19). 


DEVELOPMENT  OF  THE  THORACIC  DUCT          93 

5.  Subthymic  plexus,  passing  ventral  to  the  thymus  anlage 
(fig.  101,  20).  This  forms,  if  retained  and  further  developed  in 
the  adult,  the  occasionally  observed  "prethymic"  left  innominate 


vein 


(36) 


Any  number  of  good  examples  of  all  these  conditions  are  afforded 
by  every  13  or  14  mm.  embryo.  Thus  in  a  14  mm.  embryo 
(series  210,  slide  viii,  section  41,  X  225),  fig.  102,  direct  com- 
parison of  the  schema  shown  in  fig.  101  with  the  section  will, 
without  further  description,  make  the  arrangement  of  the  ele- 
ments composing  this  plexus  (16,  17,  18,  19,  20)  clear.  (Com- 
pare also  fig.  43  [series  189,  slide  vii,  section  10,  13.5  mm.] 
and  fig.  30  [series  210,  slide  viii,  section  39,  14  mm.]) 

The  ventral  divisions  of  this  plexus  extend  in  the  earlier  em- 
bryonic stages  (11-12  mm.)  as  a  well  developed  capillary  reticu- 
lum  into  the  upper  thoracic  region  around  and  between  oesopha- 
gus, trachea,  precardinal  veins,  vagi  and  pulmonary  arteries. 

Beginning  in  some  12  mm.  embryos,  but  more  constantly  and 
characteristically  in  the  13  mm.  stage,  certain  components  of  this 
ventral  mediastinal  venous  plexus  appear  partly  surrounded  by 
independently  developed  extraintimal  lymphatic  spaces,  which 
form  the  anlages  of  the  future  broncho-mediastinal  lymphatic 
trunk. 

Thus,  if  the  ventral  portion  of  this  venous  plexus  is  followed 
caudad  into  the  upper  thoracic  region,  into  the  area  of  the  develop- 
ing broncho-mediastinal  trunk  marked  X  in  fig.  100,  the  following 
observations  can  be  made  in  stages  of  the  proper  length,  and 
adequately  fixed  and  stained: 

1.  In  embryos  between  11  and  12  mm.  only  venous  capillaries 
are  found.  Thus  figures  103  and  104  show  transverse  sections 
of  this  part  of  the  upper  thoracic  region  in  a  12  mm.  embryo 
(series  217,  slide'  viii,  sections  21  and  29,  X  200).  The  field, 
caudal  to  oesophagus  and  aorta  (7),  contains  in  the  middle  line 
the  trachea  (9),  the  vagi  (22),  and  further  ventrad,  the  pulmonary 

38  Geo.  S.  Huntington :  '  'Contribution  to  the  topographical  anatomy  of  the  thorax 
in  the  foetus  at  term  and  the  new-born  child."  Rep.  Soc.  N.  Y.  Lying-in- 
Hospital,  1897,  p.  343,  fig.  xxxi. 


94        DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC   VESSELS 

arteries  (10).  The  branches  of  the  peritracheal  venous  plexus 
(18)  are  well  developed.  There  is  as  yet  no  indication  of  lym- 
phatic development. 

2.  In  13  mm.  embryos  certain  of  the  venous  radicles  entering 
into  this  plexus,  are  partly  surrounded  and  enveloped  by  ex- 
traintimal  lymphatic  spaces,  which  arise  independently  of  the 
venous  system,  as  the  first  anlages  of  the  future  ventral  medias- 
tinal  lymphatic  channel.     Figures  105  and  106  show  transverse 
sections  of  this  region  in  a  13  mm.  cat  embryo  (series  92,  slide 
vii,  sections  30  and  33)  in  a  magnification   of   225  diameters. 
Ventral  to  trachea  (9),  aorta  (7)  and  left  vagus  (22)  are  seen  sec- 
tions of  a  number  of  venous  radicles  (4)  of  the  ventral  mediastinal 
plexus,  some  of  which  are  partially  surrounded  by  very  small 
extraintimal  perivenous  lymphatic  anlages  (5).     Only  a  few  of  the 
most  prominent  of  these  are  indicated  in  the  figures  by  leaders, 
but  they  exist  in  many  other  parts  of  the  field. 

A  similar  section  from  another  13  mm.  embryo  (series  107, 
slide  ix,  section  40,  X  225)  is  shown  in  figure  107.  Dorsal  to 
the  pulmonary  arteries  (10),  between  them  and  the  trachea  (9) 
and  aorta  (7),  the  section  has  cut  a  prominent  extraintimal  lym- 
phatic space  (5)  in  typical  relation  to  one  of  the  radicles  (4)  of 
the  ventral  mediastinal  venous  network. 

3.  In  the  13.5  mm.  embryo  the  full  and  convincing  proof  of 
the  extraintimal  derivation  of  this  channel  is  given.     In  some 
embryos  of  the  period  the  process  is  still  seen  in  its  earlier  stages. 
Thus  figs.  108  and  109   (13.5  mm.  embryo,  series  223,  slide  x, 
sections  11  and  12,    X  225)  show  on  each  side,  ventral  to  the 
trachea  (9)  and  the  vagi  (22),  a  number  of  radicles  (4)  of  the  ven- 
tral mediastinal  capillary  plexus.     One  of  these  small  vessels, 
symmetrically  disposed  on  each  side  in  front  of  the  respective 
vagus,  is  in  process  of  being  surrounded  and  replaced  by  an  ex- 
traintimal lymphatic  space  (5). 

Other  13.5  mm.  embryos  show  a  rapid  advance  in  the  peri- 
venous  lymphatic  development. 

Fig.  110  shows  a  transverse  section  of  the  upper  thoracic 
region  of  another  13.5  mm.  embryo  (series  189,  slide  viii,  section 
35,  X  225).  Just  ventro-mesad  of  the  left  vagus  nerve  and  its 


DEVELOPMENT  OF  THE  THORACIC  DUCT  95 

encircling  vein  is  a  venous  radicle  (4)  almost  completely  sur- 
rounded by  an  extraintimal  lymphatic  space  (5)  in  the  process 
of  replacing  the  atrophying  vein  with  which  it  is  so  closely  asso- 
ciated. The  same  structures  (4,  5}  are  seen  still  more  clearly 
defined  in  the  corresponding  position  on  the  right  side  of  the 
embryo. 

Comparison  with  the  corresponding  sections  just  given  in  figures 
103  to  109  show  that  the  extraintimal  anlage  of  the  earlier  stages, 
developed  along  the  identical  venous  radicle,  has  increased  in  the 
13.5  mm.  stage,  so  as  to  nearly  envelop  the  vein,  and  that  the 
latter,  if  followed  cephalad  and  caudad,  is  now  separated  from 
the  functional  venous  channels  of  this  region  and  is  in  the  process 
of  further  recession  and  degeneration  as  the  lymphatic  perivenous 
space  enlarges  and  more  and  more  replaces  the  antecedent  venous 
channel.  The  vein  in  question  in  the  older  embryo  (series  189) 
appears  collapsed  and  shrunken,  and  contains  only  a  few  degen- 
erating red  blood  cells.  In  the  same  situation  on  the  right  side 
of  fig.  110  (series  189,  slide  viii,  section  35),  the  section  has  cut 
the  corresponding  vein  and  the  enveloping  extraintirr  al  space  at 
right  angles,  so  that  the  central  kernel  of  the  shrinking  vein  (4), 
still  containing  a  few  degenerating  red  blood  cells,  is  nearly  com- 
pletely surrounded  by  the  replacing  extraintimal  lymphatic  (5), 

Fig.  Ill  shows  the  following  section  of  the  same  embryo  (series 
189,  slide  viii,  section  36),  magnified  225  diameters,  in  a  larger 
field  which  gives  the  topographical  relations  and  may  serve  in 
in  the  orientation  of  the  succeeding  plates.  The  ventral  circum- 
ference of  the  oesophagus  (8)  and  the  aorta  (7)  are  seen  dorsally. 
The  trachea  (9],  with  the  vagi  (22}  on  either  side,  occupies  the 
central  area.  Ventrally  are  the  two  pulmonary  arteries  (10). 
The  section  is  a  most  important  one  in  interpreting  the  early 
histogenetic  stages  of  the  broncho-mediastinal  lymphatic  trunk 
and  its  relation  to  the  embryonic  mediastinal  venous  plexus. 
The  same  venous  radicle  (4),  ventral  to  the  vagus  (22),  already 
noted  in  the  preceeding  section  (fig.  110),  is  seen  on  each  side. 
On  the  left  side  it  has  been  cut  obliquely  by  the  plane  of  the 
section,  and  hence  shows  a  segment  of  considerable  length,  as 
a  practically  empty  and  partially  collapsed  endothelial  bag  (4), 


96        DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC    VESSELS 

surrounded  by  the  extraintimal  lymphatic  space  (£).  On  the 
right  side  of  the  embryo  the  corresponding  venous  radicle  (4) 
and  the  perivenous  lymphatic  anlage  (5}  have  been  again  cut 
more  at  right  angles,  so  that  the  envelopment  of  the  former  by 
the  latter  can  be  clearly  traced  nearly  throughout  the  entire  cir- 
cumference. 

Fig.  11 1 A  shows  the  decadent  vein  and  the  replacing  extrainti- 
mal lymphatic  on  the  left  side  of  this  section  in  a  higher  magnifi- 
cation, (  X  300).  The  structure  of  the  collapsed  venous  endothelial 
tube,  and  the  beginning  development  of  endothelial  character  in 
the  mesodermal  cells  limiting  the  perivenous  extraintimal  lym- 
phatic anlage,  can  be  here  clearly  made  out. 

Figs.  112  to  116  show  the  five  succeeding  sections  of  the  same 
embryo  (series  189,  slide  viii,  sections  37  to  41  inclusive)  in  a 
magnification  of  225  diameters. 

I  publish  this  series  of  plates  in  order  to  prove  on  the  one  hand 
that  the  extraintimal  lymphatic  anlages  can  be  followed  with 
certainty  and  accuracy  in  their  relation  to  the  contained  decadent 
venule  for  longer  or  shorter  distances,  and  that,  on  the  other 
hand,  they  are,  in  these  earlier  stages,  still  isolated  and  not  yet 
continuous  with  similar  anlages  in  adjacent  areas.  They  form, 
in  other  words,  in  these  earlier  periods,  detached  links  of  a  lym- 
phatic chain,  not  yet  united  to  each  other  to  form  the  continuous 
channel  of  the  later  stages. 

In  figs.  112,  113  and  114  (sections  37,  38  and  39)  beautiful  and 
clear  pictures  of  the  atrophying  central  venule  (4)  and  the  peri- 
venous extra-intimal  lymphatic  space  (5)  are  found  on  both  sides 
in  the  typical  situation  noted  in  the  preceding  sections,  with 
which  they  of  course  can  easily  be  coordinated  by  simple  com- 
parison. 

Sections  38  and  39  (figs.  113  and  114)  are  particularly  instruc- 
tive inasmuch  as  the  detached  central  vein  (4)  on  the  left  side 
still  contains  a  few  degenerating  red  blood  cells,  while  its  former 
connection  with  the  valid  and  functional  venous  plexus  around 
the  left  vagus  nerve  can  still  be  faintly  traced. 

In  section  40  (fig.  115)  the  atrophying  vein  (4)  and  the  sur- 
rounding lymphatic  (5)  of  the  left  side  appear  divided  into  two 


DEVELOPMENT  OF  THE  THORACIC  DUCT  97 

components.  On  the  right  side  the  corresponding  structures  end 
blindly. 

In  the  following  section  (41,  fig.  116)  the  left  venule  and  lym- 
phatic also  terminate  almost  entirely  in  the  indifferent  mesoder- 
mal  tissue,  only  a  small  remnant  (4,  5)  persisting  between  trachea 
and  left  vagus.  This  disappears  entirely  in  the  following  section. 

The  succeeding  stage  (14  mm.)  shows  the  same  lymphatic 
anlages  surrounding  and  replacing  the  atrophying  venules  of  the 
ventral  mediastinal  plexus  in  still  higher  development.  It  ap- 
pears from  the  study  of  numerous  embryos  of  this  length,  that 
the  average  14  mm.  stage  represents  the  point  in  the  lymphatic 
ontogenesis  of  this  region  at  which  the  pictures  are  most  strik- 
ing. The  central  kernel  of  the  decadent  vein  is  still  large  and, 
in  places,  as  yet  incompletely  separated  from  the  definite  venous 
channels.  At  the  same  time  the  perivenous  lymphatic  space  has 
acquired  an  increased  lumen  and  hence  the  two  combined  struc- 
tures occupy  a  relatively  large  field. 

Thus  figs.  117  to  122  show  transverse  sections  of  the  ventral 
thoracic  region  in  a  14  mm.  cat  embryo  (series  212,  slide  x,  sec- 
tions 4,  5,  6,  7,  10  and  11,  X  225).  In  figs.  117  and  118  the 
developing  lymphatic  anlages  (5)  of  the  broncho-mediastinal 
trunk  can  fce  readily  recognized  and  present  the  same  relation 
to  the  atrophying  venules,  which  they  surround,  as  in  the  sections 
of  the  preceding  series  just  described  and  figured.  In  contra- 
distinction to  these  structures  the  components  of  the  permanent 
functional  venous  plexus  of  this  region  (32)  form  well-differen- 
tiated vascular  channels. 

In  fig.  119  (series  212,  slide  x,  section  6)  the  scattered  lym- 
phatic anlages  occupying  in  the  two  preceding  sections  the  space 
between  the  left  pulmonary  artery  (10)  and  the  left  vagus  (22), 
with  its  accompanying  ventral  mediastinal  vein  (32),  are  gathered 
together  into  a  more  extensive  elongated  space  (5).  In  the 
interior  of  this  is  seen  the  endothelial  bag  of  the  empty  and 
atrophying  venule  (4)  which  the  lymphatic  is  about  to  replace. 
The  vein  remnant  is  almost  completely  surrounded  by  the  lym- 
phatic space  and  only  connected  to  the  latter's  endothelial  wall 
by  a  bridge  at  one  point.  Other  areas  of  similar  lymphatic  devel- 


98         DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC    VESSELS 

opment  are  seen  on  the  opposite  side  (4-6)  and  (not  labelled)  in 
the  center  of  the  field,  but  the  structures  on  the  left  side  are, 
as  in  the  earlier  stages  (cf.  series  189)  better  developed  and 
larger. 

The  succeeding  figures,  120,  121  and  122  (sections  7,  10  and 
11)  show  the  same  structures,  which  can  be  distinctly  followed 
for  some  distance  caudad  of  the  last  section  figured.  In  fig.  122  the 
original  connection  of  the  large  upper  venous  kernel  of  the  left  side 
(4)  with  one  of  the  components  of  the  peritracheal  venous  plexus 
(18}  is  still  suggested  by  the  arrangement  of  the  adjacent  cells, 
although  the  degenerating  vein  has  been  cut  off  from  all  actual 
communication  with  the  permanently  valid  channels  of  the 
mediastinal  venous  plexus. 

The  14  mm.  stage  is  so  important,  and  the  results  gained  by 
the  examination  of  a  large  number  of  embryos  so  conclusive  in 
respect  to  the  true  ontogenesis  of  the  systemic  lymphatic  channels, 
that  I  have  selected  a  well  marked  example  and  publish  here 
eighteen  consecutive,  or  nearly  consecutive,  sections  from  the 
same  individual.  I  do  this  in  order  to  show  the  extent  to  which 
extraintimal  perivenous  lymphatic  development  has  proceeded 
in  this  stage,  in  respect  to  the  length  of  the  resulting  segments  of 
the  future  lymphatic  channel,  still  separated  from  each  other, 
and  to  accentuate,  by  a  large  number  of  successive  illustrations 
from  the  same  embryo,  the  histogenesis  of  the  lymphatic  anlages 
in  their  relation  to  the  decadent  embryonic  venules  which  they 
eventually  entirely  replace.  The  conception  involved  by  the 
theory  of  extraintimal  systemic  lymphatic  development  has 
proved  apparently,  to  judge  from  published  comments,  difficult 
to  understand  in  some  laboratories  from  the  histo-mechanical 
standpoint.  The  following  eighteen  reproductions  of  sections 
of  a  14  mm.  embryo  (series  214,  slide  xiii)  surely  explain,  with- 
out  detailed  description,  the  principles  underlying  lymphatic 
ontogenesis  in  the  mammalian  embryo.  I  very  gladly  welcome 
the  opportunity,  which  this  series  of  Wistar  publications  offers, 
for  presenting  them. 

The  plates  comprised  in  this  group  are  shown  in  order  cephalo- 
caudad  in  figures  123  to  141  inclusive.  In  all  of  them  the  ex- 


PEVELOPMENT  OF  THE  THORACIC  DUCT          99 

traintimal  lymphatic  anlages  of  the  broncho-mediastinal  trunk 
are  indicated  by  the  leader  5,  while  the  included  remnant  of  the 
atrophying  embryonic  vein  is  labelled  4,  as  in  the  preceding 
and  following  figures. 

Figs.  123,  124, 125  and  126  (sections  4, 5,  6  and  7)  show  well  the 
relation  of  the  venule  (4),  undergoing  atrophy  and  replacement 
by  the  extraintimal  lymphatic  space  (5),  to  the  permanent 
venous  channels  of  the  mediastinal  plexus.  Thus  in  fig.  123  the 
dorsal  large  lighter  area  marked  4  is  the  blind  cephalic  end  of  a 
venule  which  is  nearly  detached  from  the  permanent  peritracheal 
(18}  and  ventral  mediastinal  (32)  venous  channels,  and  which  in 
the  succeeding  sections  is  seen  to  be  partially  surrounded  by  the 
extraintimal  lymphatic  space  (5)  eventually  designed  to  replace 
it  entirely. 

In  figure  124  (section  5)  this  peri  venous  space  (5)  has  developed. 
The  included  vein  (4)  is  still  partially  connected  with  the  func- 
tional peritracheal  plexus  (18).  Further  ventrad  is  another  por- 
tion of  this  same  plexus.  The  venous  kernel  here  still  contains  a 
number  of  red  blood-cells.  These  characteristic  relations  of 
developing  lymphatic  and  receding  vein  can  be  followed  clearly 
throughout  the  succeeding  sections.  The  contrast  between  the 
well  filled  permanent  veins  (e.g.,  18,  32  in  figs.  123,  124,  125 
and  126),  with  walls  fitted  closely  into  the  surrounding  mesen- 
chyme,  and  the  atrophying  venule  surrounded  by  the  extraintimal 
lymphatic  anlage,  is  striking  throughout  the  series.  Some  of  the 
sections  show  in  certain  regions  good  pictures  of  nearly  complete 
reduction  of  the  decadent  vein  to  an  insignificant  central  kernel 
of  connective  tissue  surrounded  by  the  extraintimal  lymphatic 
space;  thus,  e.g.,  figs.  137  to  141  in  the  region  ventro-mesad  to 
the  left  vagus  (22). 

The  15  mm.  stage  shows  the  developing  lymphatic  plexus  of 
the  broncho-mediastinal  trunk  further  advanced.  Figs.  142  to 
145  show  four  successive  transverse  sections  through  the  ventral 
part  of  the  upper  thoracic  region  in  a  15  mm.  cat  embryo  (series 
216,  slide  x,  sections  32,  33,  34  and  35,  X  225).  The  central 
decadent  venule  in  the  interior  of  the  developing  perivenous 
lymphatic  space  has  in  many  places  disappeared  entirely,  leav- 


100       DEVELOPMENT   OF   THE   SYSTEMIC  LYMPHATIC  VESSELS 

ing  only  the  clear  lymphatic  lumen  (5).  In  other  places  remnants 
of  the  replaced  vein  (4)  can  stiU  be  distinctly  determined.  This 
clearance  has  resulted  in  a  relative  diminution  of  the  actual  area 
of  a  cross  section  of  the  meshes  of  the  lymphatic  plexus,  since  now 
the  entire  lumen  is  given  over  to  the  newly  formed  lymphatic 
channel,  whereas  in  the  earlier  stages  its  central  area  was  still 
largely  filled  by  the  degenerating  veil.  The  lymphatic  spaces 
in  these  sections  have  increased  considerably  in  number.  (Only 
a  few  of  the  more  prominent  vessels  are  indicated  in  the  figures 
by  leaders.) 

A  transverse  section  of  this  region  in  a  15.5  mm.  cat  embryo 
(series  215,  slide  xiv,  section  31,  X  225)  is  shown  in  a  fig.146. 
The  preceding  more  diffuse  lymphatic  plexus  of  the  earlier  stages 
is  condensed  to  a  much  smaller  mesenchymal  network.  In  a 
few  of  the  larger  meshes  a  remnant  of  the  former  central  vein  (4) 
can  still  be  traced  as  a  solid  plug  of  mesoderm  surrounded  by  the 
lymphatic  channel  (5}. 

In  general  the  15  and  15.5  mm.  embryos  of  the  cat  represent 
the  stages  in  the  development  of  the  broncho-mediastinal  trunk 
in  which  the  histological  pictures  of  the  lymph  channels  are  least 
distinct  and  striking.  This  is  due  to  the  fact  that  on  the  one 
hand  they  have  lost  the  central  venous  kernel  around  which  they 
were  originally  developed  through  confluence  of  extraintimal 
spaces,  and  which  gave  to  the  combined  structures  their  area 
on  section  and  their  distinctive  appearance  in  the  earlier  (13.5 
and  14  mm.)  stages,  while  on  the  other  hand  the  independent 
growth  and  enlargement  of  the  lymph  channels  proper  begins  in 
the  16  mm.  stage.  In  some  embryos,  measuring  16  mm.,  the 
appearances  characteristic  of  the  15  mm.  and  15.5  mm.  stages  are 
still  encountered.  Thus  fig.  147  shows  a  transverse  section 
through  the  ventral  area  of  the  upper  thoracic  region  in  a  16  mm. 
embryo  (series  230,  slide  xii,  section  25,  X  '225).  The  corre- 
spondence of  the  histological  picture  to  that  presented  by  the 
15  mm.  or  15.5  mm.  embryo  is  seen  by  comparison  with  series 
215  and  216  (figs.  142  to  146). 

The  majority  of  16  mm.  embryos  show,  however,  a  marked 
advance  in  the  independent  growth  of  the  lymphatic  channels. 


DEVELOPMENT  OF  THE  THORACIC  DUCT         101 

which  have  become  fully  established.  Their  lumen  now  appears 
for  the  most  part  entirely  cleared  of  the  remnants  of  the  decadent 
venules  originally  contained  therein.  In  only  a  few  instances 
does  the  original  vein  kernel  appear  reduced  to  an  insignificant 
rudiment.  The  resulting  plexus  of  the  broncho-mediastinal  lym- 
phatic duct  fills  the  typical  position  occupied  in  the  earlier  stages 
by  the  extensive  preceding  perivenous  lymphatic  reticulum. 
Thus  figs.  148-153  give  transverse  sections  through  the  ventral 
part  of  the  upper  thoracic  region  in  another  16  mm.  cat  embryo 
(series  222,  slide  X,  sections  1,  2,  3,  10, 15  and  16,  X  225).  This 
embryo  affords  remarkably  clear  pictures  of  the  fully  devel- 
oped lymphatic  plexus  of  the  ventral  or  broncho-mediastinal 
trunk. 

Figs.  148  and  153  (sections  1  and  16)  give  the  topographical 
pictures  of  the  entire  region  involved.  The  broncho-mediastinal 
lymphatic  plexus  (37)  is  fully  developed  in  the  typical  area  between 
the  trachea  (8)  and  vagi  (22}  dorsally  and  the  pulmonary  arteries 
(10)  ventrally.  The  lymphatic  spaces  possess  a  clear  lumen  and 
distinct  endothelial  walls.  The  remnants  of  the  degenerating 
ventral  mediastinal  venous  plexus  which  they  have  replaced  have 
almost  entirely  disappeared.  Only  slight  traces  of  them  are 
still  to  be  seen  here  and  there.  In  the  main  the  lymphatic  chan- 
nels are  clear  of  venous  kernels  and  form  a  rich  interlacing  lym- 
phatic plexus.  The  central  field  contains  the  oesophagus  (8), 
aorta  (7)  and  part  of  the  medial  circumference  of  the  left  praecava 
(6).  Dorsally  on  the  right  side  the  right  azygos  vein  (3)  and 
sympathetic  nerve  (1)  appear,  while  on  the  left  side  the  section 
includes  the  cephalic  part  of  the  azygos  segment  of  the  left  thoracic 
duct  (36). 

Sections  2,  3,  10  and  15  of  the  same  slide  are  shown  in  their 
ventral  portions  in  figs.  149  to  152.  They  all  exhibit  the  extent 
and  continuity  of  the  broncho-mediastinal  lymphatic  channel 
complex  in  this  stage.  The  figures  are  not  leadered,  but  the 
individual  structures  can  be  readily  identified  by  reference  to 
the  topographical  figures  148  and  153. 

The  succeeding  stages  are  characterized  by  a  condensation  of 
the  extensive  lymphatic  plexus  of  the  typical  16  mm.  and  17  mm. 


102 

embryos  into  the  more  definite  channel  of  the  broncho-mediastinal 
trunk  with  larger  caliber. 

Figs.  154  to  158  show  the  region  of  the  broncho-mediastinal 
channel  in  four  successive  sections  in  a  20  mm.  cat  embryo 
(series  241,  slide  xix,  sections  19,  20,  21  and  22,  X  225).  Fig. 
154  again  gives  a  topographical  view  of  the  entire  field,  while 
the  same  is  cut  down  to  the  ventral  portion  in  the  remaining  plates. 
In  all  the  multi-meshed  lymphatic  plexus  of  the  preceding  stage 
is  replaced  by  the  more  definite  and  larger  channel  of  the  broncho- 
mediastinal  trunk  proper  (37),  in  the  classical  situation  between 
the  pulmonary  arteries  (10)  ventrally  and  the  trachea  (9),  vagi 
(22)  and  permanent  ventral  mediastinal  veins  (18)  dorsally. 

This  stage  marks  the  practical  attainment  of  adult  conditions 
for  the  lymphatic  channel  of  the  broncho-mediastinal  trunk,  and 
from  this  period  on  its  further  development  is  merely  a  question 
of  continued  growth  and  adaptation  to  the  environment  in  es- 
tablishing secondary  connections  with  the  tributary  channels, 
developed  independently,  the  preazygos  segment  of  the  thoracic 
duct,  and  (usually)  the  ventral  prolongation  of  the  subclavian 
approach  of  the  jugular  lymph  sac. 

As  will  be  seen  from  the  foregoing  analysis  of  the  development 
of  the  broncho-mediastinal  lymphatic  trunk  in  embryos  of  the 
cat,  the  principles  of  mammalian  systemic  lymphatic  ontogenesis 
defined  in  Part  I  of  this  memoir  are  consistently  sustained  by 
the  actual  evidence  afforded.  The  development  of  the  perive- 
nous  extraintimal  anlages  which  form  the  basis  for  the  subse- 
quent evolution  of  the  systemic  lymphatic  channels,  is  a  uniform 
and  remarkably  consistent  process. 

The  existence  of  these  spaces  in  this  and  other  regions  of  the 
embryo  has  been  so  often  denied  by  recent  contributors  to  the 
subject,  or,  if  admitted,  explained  in  every  possible  way  except 
through  the  correct  interpretation,  that  I  publish  in  this  paper 
a  series  of  micro-photographs  of  a  considerable  number  of  sec- 
tions taken  from  embryos  of  all  the  important  stages.  Of  course 
these  observations  could  be  indefinitely  multiplied.  The  larger 
the  embryological  collection,  and  the  better  the  individual  prep- 
arations are  fixed  and  stained,  the  more  conclusive  will  be  the 


DEVELOPMENT  OF  THE  THORACIC  DUCT         103 

results  of  a  careful  examination  of  lymphatic  development  along 
the  lines  here  indicated. 

No  competent  and  impartial  observer  can  mistake  the  signifi- 
cance of  the  conditions  here  shown.  Every  stage  of  the  process 
can  be  followed  in  detail.  The  behavior  of  the  decadent  embry- 
onic vein,  and  its  relation  to  the  enveloping  extraintimal  lymphatic 
channel,  are  absolutely  demonstrated.  The  endothelium  of  the 
shrinking  vein  has  no  share  in  furnishing  the  independent  lym- 
phatic endothelium  of  the  replacing  mesenchymal  space,  and 
nowhere,  in  the  entire  process,  is  there  the  faintest  suggestion 
of  an  "  out-bud"  or  of  a  "  splitting  off"  from  the  circumference  of 
an  otherwise  valid  embryonic  vein  of  "lymphatic"  or  aveno- 
lymphatic"  anlages. 

It  is  evident  in  comparing  a  number  of  embryos  between  13. 
and  16  mm.,  crown-rump  measure,  that  the  extensive  area  occu- 
pied by  the  lymphatic  anlages  in  the  earlier  stages  (13  mm.,  13.5 
mm.  and  14  mm.)  is  due  to  the  relatively  large  ske  of  the  central 
decadent  vein.  In  the  earlier  stages  (e.g.,  figs.  Ill,  112,  113,  114, 
119,  121,  125,  126,  127,  series  189,  212  and  214)  the  evacu- 
ated and  abandoned  vein  appears  as  a  wide  loose  and  partially 
collapsed  endothelial  bag,  surrounded  by  a  narrow  extraintimal 
lymphatic  space,  with  but  as  yet  indifferently  defined  endothelial 
lining,  continuous  at  one  or  more  points  with  the  external  surface 
of  the  endothelium  of  the  degenerating  vein.  As  development 
proceeds  the  actual  perivenous  lymphatic  spaces  increase  but  they 
concentrate  and  narrow  down  on  the  contained  venous  kernel, 
and,  as  the  latter  continues  to  decrease  in  size  and  finally  become 
completely  eliminated,  the  resulting  clear  lymphatic  channel  oc- 
cupies relatively  less  space  than  that  filled  in  the  earlier  stages 
by  the  decadent  venule  and  the  early  surrounding  lymphatic 
anlage  combined. 

Thus  in  the  15,  15.5  and  in  some  16  mm.  embryos  (figs.  142, 
143,  144,  145,  146,  and  147,  series  216,  215  and  230),  while  the 
actual  lumen  of  the  lymphatic  channel  has  increased  that  of  the 
enclosed  and  abandoned  vein  has  correspondingly  receded  to  an 
insignificant  remnant,  which  projects  into  the  lymphatic  space 
from  a  narrow  pedicle  attached  to  the  latter's  endothelial  lining. 


104      DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC    VESSELS 

Consequently,  in  the  pictures  of  the  earlier  stages  (13,  13.5  and 
14  nun.  embryos)  the  area  occupied  by  the  still  capacious  aban- 
doned venous  channel,  combined  with  that  of  the  relatively  narrow 
enveloping  lymphatic  space,  appears  larger  and  more  prominent 
than  in  the  later  periods  (15,  15.5  mm.)  in  which  the  permanent 
lymphatic  channel  and  its  reduced  venous  kernel  occupies  less 
histological  territory. 

It  should  also  be  noted  that  in  the  earlier  stages  (13,  13.5, 
14  mm.)  the  perivenous  extraintimal  lymphatic  network  is  more 
diffuse  and  redundant  than  in  the  later  stages  (15,  15.5,  16  mm.). 
This  early  plexiform  lymphatic  reticulum  is  subsequently  con- 
densed into  more  limited  and  better  defined  lymph  channels,  in 
exact  conformation  to  the  processes  observed  in  the  haemal 
vascular  development,  in  which  the  definite  blood  channels 
crystallize  along  main  lines  out  of  an  antecedent  indefinite  and 
more  diffuse  plexus.  The  result  of  this  genetic  process  is  strik- 
ing in  tracing  developing  lymphatics  through  successive  stages. 
Thus  in  the  region  here  under  discussion  the  pictures  offered  by 
the  13,  13.5  and  14  mm.  embryos  are  more  conclusive  than  those 
furnished  by  the  15  and  15.5  mm.  stages  in  reference  to  the  gene- 
sis of  the  lymphatic  channels.  In  the  former,  the  lymphatic 
anlages  and  the  decadent  venules  around  which  they  develop  are 
taken  together,  relatively  larger  and  more  numerous,  and  hence 
easier  to  recognize.  In  the  latter,  this  early  redundant  perive- 
nous lymphatic  plexus  has  been  replaced  by  a  relatively  smaller, 
but  much  more  definite  and  distinct  channel,  occupying,  however, 
always  a  part  of  the  area  filled  in  the  earlier  stages  by  the  less 
circumscribed  antecedent  lymphatic  plexus  with  its  contained 
remnants  of  abandoned  embryonic  veins.  I  lay  special  stress  on 
this  fact,  because  it  is  absolutely  necessary  to  take  it  into  account 
in  comparing  stages  between  13.5  and  15.5  mm.  In  the  latter 
stage  the  final  lymphatic  anlages  have  definitely  formed  and  have 
reached  the  relation  to  adjacent  main  venous  lines  which  they 
henceforth  are  to  occupy.  The  further  growth  and  enlargement 
of  these  channels  begins  in  the  16  mm.  embryo,  and  proceeds 
from  this  point  on,  in  many  regions  at  the  expense  of  the  adjacent 
embryonic  vein  undergoing  atrophy. 


DEVELOPMENT    OF    THE    THORACIC    DUCT  105 

The  only  conclusion  which  seems  to  me  to  be  warranted  by 
actual  observation  is  that  certain  embryonic  veins  form,  during 
the  process  of  their  atrophy  and  final  elimination  from  the  definite 
venous  organization,  the  supporting  lines  along  which  certain 
of  the  peri  venous  extraintimal  lymphatic  anlages  first  develop. 

The  fact  that  numerous  early  embryonic  venous  channels, 
large  and  small,  atrophy  and  disappear  during  the  normal  course 
of  subsequent  development,  appears  to  afford  a  more  favorable 
field  for  the  greater  development  of  the  adjacent  mesenchymal  in- 
intercellular  spaces,  so  that  these  enlarge  more  rapidly,  as  the  corre- 
lated vein  recedes.  This  relationship  appears,  however,  to  be 
based  exclusively  on  the  physical  and  mechanical  ad  vantages  which 
the  abandoned  and  shrinking  primary  venous  line  affords  to  the 
adjacent  mesenchymal  spaces  for  more  rapid  enlargement,  in 
the  sense  of  replacing  the  disappearing  vein  and  occupying  second- 
arily the  space  formerly  filled  by  the  haemal  channel.  This  is 
evidently  an  important  factor  in  determining  the  size  and  extent 
of  the  final  lymphatic  channel  resulting  from  the  confluence  of 
the  originally  separate  and  independent  perivenous  anlages. 
Consequently,  in  the  adult,  the  largest  and  best  defined  systemic 
lymphatic  vessels  either  accompany  reduced  adult  remnants  of  a 
relatively  larger  embryonic  venous  channel,  or,  in  case  of  the 
latter's  entire  default,  topographically  replace  the  same.  Now, 
while  this  relation  manifests  itself  strikingly  in  many  parts  of 
the  body,  it  is  quite  evident  that  the  development  of  lymphatic 
channels  occurs  in  other  parts  independently  of  preceding  veins, 
by  the  confluence  of  independent  intercellular  mesenchymal 
spaces. 

The  cat  may,  and  does,  differ  in  its  details  of  lymphatic  develop- 
ment, and  in  its  adult  lymphatic  organization,  from  the  condi- 
tions obtaining  in  many  other  mammalian  forms.  In  fact,  even 
in  the  present  very  incomplete  state  of  our  knowledge  of  the  com- 
parative anatomy  of  the  mammalian  lymphatic  system,  we 
realize  that  what  we  regard  as  the  mammalian  ground  plan  of 
lymphatic  organization  may  in  certain  genera  undergo  great  and 
far-reaching  modifications,  as  for  example  the  conditions  deter- 


106      DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC    VESSELS 

mined  by  Silvester37  for  the  whole  group  of  the  Cebidae,  and  those 
found  by  myself  in  Macropus  rufus.  And  yet  these  differences, 
established  and  maintained  within  the  natural  limits  of  the 
mammalian  class,  cannot,  in  whatever  degree  they  actually  exist, 
in  individual  forms  be  basic.  In  any  given  mammalian  type, 
the  systemic  lymphatic  vessels,  whatever  their  adult  relation  to 
and  connection  with  the  venous  system  may  be,  must  develop 
in  accordance  with  a  genetic  ground  plan  common  to  all  mammalia. 


37  C.  F.  Silvester.  "On  the  Presence  of  Permanent  Lymphatico-Venous 
Communications  at  the  Level  of  the  Renal  Veins  in  Adult  South  American 
Monkeys." 

Anat.  Am.,  Erganzungsh.  z.  37.  Bd.,  Vevh.  Anat.  Ges.,  24  Vevs.,  Brussels, 
1910,  S.  111-114. 


PART  II     PLATES 

FIGURES  100  TO  158 


FIGURE  100 


100    Transverse  section  of  upper  thoracic  region  in  a  12  mm.  cat  embryo  (series 
78f  slide  IX,  section  5),  X  50. 

1  Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Precardinal  or  precava,  resp.  azygos  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10  Pulmonary  artery. 

16  Dorso-medial  somatic  venous  tributaries. 

22  Vagus. 

31  Primitive  ulnar  veno-lymphatic. 

33  Subclavian  artery. 

48  Right  auricle. 

49  Left  auricle. 

50  Right  ventricle 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  at 


50 


100 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURE  101 

101     Schema  of  venous  plexuses  of  left  side  in  lower  cervical  region  of  cat  embryo 
between  13  mm.  and  14  mm.  crown-rump  measure  in  transverse  section. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

16  Dorso  medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus, 

18  Feritracheal  venous  plexus. 

19  Suprathymic  venous  plexus. 

20  Subthymic  venous  plexus. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 
20  Common  jugular  vein. 


THK   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   52 


101 


MEMOIR  NO.   1,    HUNIINQTON,    1911 


FIGURE  102 

102    Transverse  section  of  lower  cervical  region  in  a  14  mm.  cat  embryo  (series 
210,  slide  VIII,  section  41),  X  225. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

16  Dorso-medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus. 

18  Peritracheal  venous  plexus. 

19  Suprathymic  venous  plexus. 

20  Subthymic  venous  plexus. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 

24  Thyrocervical  artery. 

25  Internal  jugular  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  53 


W&S&F 

.-k^  Ai-***  ¥*  t     9,0* , 


fcyiB  !i  /js 

%W>"^  jF 

JSJi^&.tr    JV.*  _*!•', 


.v,  *  :  >',;^^r 

/  4«'^-v*  «s_-v>r^% 


E*^;  ;,X?    '    ,.-V»  *.-H 

iWaw  •-."'  -rV, 


-'•'/::  ,.>*^s 

»'.  •-.     *-V,*ji*1^0l! 


102 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  103  AND  104 

103  Transverse  section  of  ventral  part  of  upper  thoracic  region  in  a  12  mm.  cat 
embryo  (series  217,  slide  VIII,  section  21) ,  X  200. 

104  Same,  section  29. 

7  Aorta. 

9  Trachea. 

10  Pulmonary  artery. 

18  Peritracheal  venous  plexus. 

22  Vagus. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   51 


104 


MEMOIR    NO.    1,    HUNTINGTON,    1911 


FIGURES  105  AND  106 

105  Transverse  section  of  ventral  part  of  upper  thoracic  region  in  a  13  mm. cat 
embryo  (series  92,  slide  VII,  section  30),  X  225. 

106  Same,  section  33. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 
22    Vagus. 


TIIK   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE   55 


106 


MKMOIK   NO.    1,   HttNTINGTON,    1911 


FIGURE  107 

107    Transverse  section  of  ventral  part  of  upper  thoracic  region  in  a  13  mm.  cat 
embryo  (series  107,  slide  IX,  section  40) ,  X  225. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 
7     Aorta. 
9    Trachea. 
10     Pulmonary  artery. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  56 


107 


MEMOIR    XO.    1,    HUNTINGTON,    1911 


FIGURES  108  AND  109 

108  Transverse  section  of  ventral  part  of  upper  thoracic  region  in  a  13.5  mm. 
cat  embryo  (series  223,  slide  X,  section  11),  X  225. 

109  Same,  section  12. 

4  -  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 
7     Aorta. 
9     Trachea. 
22    Vagus. 


THE   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE   57 


MEMOIR   NO.   1,   HONTINGTON,    1911 


FIGURES  110  AND  111A 

110  Transverse  section  through  ventral  part  of  upper  thoracic  region  in  a  13.5 
mm.  cat  embryo  (series  189,  slide  VIII,  section  35) ,  X  225. 

111  A    Left  part  of  section  36  of  same  embryo,  shown  in  the  following  figure 
111.  X300. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  orperivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 


THE  SYSTEMIC   LYMPHATIC  VESSELS 


PLATE  58 


FIGURE   111 

111     Transverse  section  through  ventral   part  of  upper  thoracic  region  in  a 
13.5  mm.  cat  embryo  (series  189,  slide  VIII,  section  36),  X  225. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10    Pulmonary  artery.       '    . 
22     Vagus. 


THE   SYSTEMIC    LYMPHATIC   VESSELS, 


PLATE   59 


Rw9L*«ftSr*?7  *il 


MKMOlIi    XO.    1,   HUNTINGTOX,    1911 


1    11 


FIGURES  112  AND  113 

112  Same,  section  37,  X  225. 

113  Same,  section  38,  X  225. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space    surrounding  degener- 

ating embryonal  vein. 


THE  SYSTEMIC   LYMPHATIC   VESSELS 


PLATE 


113 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  116  AND  117 

116  Same,  section  41,  X  225. 

117  Transverse  section  through  ventral  part  of  upper  thoracic  region  in  a  14 
mm.  cat  embryo  (series  212,  slide  X,  section  4.) ,.  X  22.5. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

7     Aorta. 

9    Trachea. 
10    Pulmonary  artery. 
22    Vagus. 
32     Ventral  mediastinal  venous  plexus. 


THE   SYSTEMIC    LYMPHATIC  VESSELS 


PLATE  62 


io -*r 


10 


117 


MKMOIIt    NO.    1,    HUNTIXGTON,    1911 


FIGURES  118  AND  119 

118  Same,  section  5. 

119  Same,  section  6. 

Right  precaval  vein. 

Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5     Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 
ing embryonal  vein. 
7    Aorta. 
9    Trachea. 
10     Pulmonary  artery. 
22    Vagus. 
32    Ventral  mediastinal  venous  plexus. 


Till:   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   63 


119 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  120  AND  121 

120  Same,  section  7. 

121  Same,  section  10. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

7     Aorta 

9    Trachea. 
10     Pulmonary  artery. 
22    Vagus. 
32    Ventral  mediastinal  venous  plexus. 


TIIK   SYSTEMIC   LYMPHATIC   VESSELS 


//&  i,v  V  <™*J*  's&F   *'  ,    >  RtftZftiy™ 

V-  ^//-v '? '/;  ?&/&&     '£?•'. ' £f£'*flSK- 
\£&$?^j  ^'**  *^ffi£-  w .  3  ^Xf^' 

-  j^ir:'  »« jfc&v&S^*>fcy^--5r-7**9^; 


10 


10 


121 


MKMOIH    NO.    1,    HUNT1NOTON,    Hill 


FIGURES  122  AND  123 

122  Same,  section  11. 

123  Transverse  section  through  ventral  part  of  upper  thoracic  region  in  a  14  mm. 
cat  embryo  (series  214,  slide  XIII,  section  4)  X  225. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

7  Aorta. 

9  Trachea. 

10  Pulmonary  artery. 

18  Peritracheal  venous  plexus. 

22  Vagus. 

32  Ventral  mediastinal  venous  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   65 


*8lw<S&tt&&fisKffi 

.<J'9jtj*Jlf^  &  «£•/      *  V%^V 


MEMOIR    NO.    1,    HUNTINGTON,    1911 


FIGURES  124  AND  125 

124  Same,  section  o. 

125  Same,  section  6. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

7  Aorta. 

9  Trachea. 

10  Pulmonary  artery. 

18  Peritracheal  venous  plexus. 

22  Vagus. 

32  Ventral  mediastinal  venous  plexus. 


THK   SYSTEMIC   LYMPHATIC   VKSSKI.S 


PLATE 


10 


10 


125 


MKMOIK    NO.    1,   HUNTINGTON,    1911 


FIGURES  126  AND  127 

126  Same,  section  7. 

127  Same,  section  8. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

o    Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 
ing embryonal  vein. 
7    Aorta. 
9    Trachea. 
10    Pulmonary  artery. 
22    Vagus. 
32    Ventral  mediastinal  venous  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   67 


22 


532 


127 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  128  AND  129 

128  Same,  section  10. 

129  Same,  section  11. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

7    Aorta. 

9    Trachea. 
10    Pulmonary  artery. 
22    Vagus. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  88 


9 A?  •<     '    »^**   t   -V$,< 

'fXT»'.  %>^v  ^  »> '>, 

f*   **  "  _<» f  «.*  *^-^ri-  < «l 


129 


MEMOIR    NO.    1,   HUNTINGTOX,    1911 


FIGURES  130  AND  131 

130  Same,  section  14. 

131  Same,  section  15. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

6  Precardinal  or  precava,  resp.  azygos  of  left  side. 

7  Aorta. 

9    Trachea. 
10    Pulmonary  artery. 
22    Vagus. 


THE   SYSTEMIC    LYMPHATIC   YKSSKLS 


PLATE   69 


MEMOIR    NO.    1,    HUNTINGTON,    1911 


FIGURES  132  AND  133 

132  Same,  section  16. 

133  Same,  section  17. 

3  Right  precaval  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 
9    Trachea. 
10    Pulmonary  artery. 
22    Vagus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   70 


133 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  134  AND  135 

134  Same,  section  18. 

135  Same,  section  19. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 
9    Trachea. 
10     Pulmonary  artery. 
22    Vagus. 


THE   SYSTEMIC    LYMPHATIC    VESSELS 


•*;^j^§|i^^ 

'+  ~i f »  %."   '  * *>*\ ' }'*.  " p  ' . • ' 


135 


MBMOIR   NO.    1,   HUNTINGTON,    191! 


FIGURES  138  AND  139 

138  Same,  section  22. 

139  Same,  section  23. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

o     Extraintimal   or   perivenous   lymphatic   space   surrounding    degen- 
erating embryonal  vein. 

6  Precardinal  or  precava  of  left  side. 

7  Aorta. 

9    Trachea. 
10     Pulmonary  artery. 
22    Vagus. 


Tlfi:    SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   73 


?/*••  *fL'J\**-WJ 

it.  V  •  »V<  />  '»*  «f  tV  . 
i  Al  -cL*-  v/5  «/  ^>  »• 
.^i'  •  V'.Wi^  ',••! 


10 


138 


r^-*1  \%-  ^  %1«-^»*S  t-i' ' **"    s  "/X 


10 


10 


139 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


140  Same,  section  24. 

141  Same,  section  25. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal    or   perivenous   lymphatic   space   surrounding   degen- 

erating embryonal  vein. 

6  Precardinal  or  precava  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10    Pulmonary  artery. 
22    Vagus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   74 


141 


MEMOIR  NO.    1,   HUNTINGTON,    1911 


FIGURES  142  AND  143 

142  Transverse  section  through  ventral  part  of  upper  thoracic  region  in  a  15 
mm.  cat  embryo  (series  216,  slide  X,  section  32),  X  225. 

143  Same,  section  33. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal   or   perivenous    lymphatic   space   surrounding    degen- 

erating embryonal  vein. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10     Pulmonary  artery. 
22    Vagus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  75 


22 


•  *  >k/*  v  *v-  >~»  *  .">*- 

-/^H^,/r.^#- .;-, 


MEMOIR  NO.    1,   HUNTINGTON,   1911 


FIGURES  144  and  145 

144  Same,  section  34. 

145  Same,  section  35. 

3  Right  precaval  vein. 

4  Atrophying  embryonal   vein,  forming  kernel    in    interior  ot  devel- 

oping and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic    space    surrounding  degen- 

erating embryonal   vein. 

6  Precardinal  or  precava  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10     Pulmonary    artery. 

18     Peritracheal  venous  plexus. 

22     Vagus. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   76 


10 


145 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  146  AND  147 

146  Transverse  section  through  ventral    part   of    upper    thoracic  region  in 
a  15.5  mm.  cat  embryo  (series  215,  slide  XIV,  section  31),  X  225. 

147  Transverse  section  through  ventral  portion  of  upper  thoracic  region  in 
a  16  mm.  cat  embryo  (series  230,  slide  XII,  section  25),  X  225. 

3  Right  precaval  vein. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

6  Precardinal  or  precava  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10     Pulmonary  artery. 

22    Vagus. 

32    Ventral  mediastinal  venous  plexus. 


THE   SYSTEMIC  LYMPHATIC   VESSELS 


PLATE  77 


.  w««rJ3*7fr  'UKSr*  %F>4n  F$Kri&  .%d 


147 


MEMOIR  NO.   1,  HUNTINGTON,   1911 


FIGURE  148 

148     Transverse  section  through  ventral  portion  of  upper  thoracic;  region 
a  16  mm.  eat  embryo  (series  222,  slide  X,  section  2),  X  225. 

1  Sympathetic  nerve. 

3  Right  Azygos  vein,  thoracic  portion. 

6  Precardinal  or  precava  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea, 

10  Pulmonary  artery. 

22  Vagus. 

36  Thoracic  duct,  azygos  segment. 

37  Broncho-mediastinal   duct. 


THE    SYSTEMIC    LYMPHATIC  VESSELS 


PLATE   78 


"'*  '%•  •  u  * 

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•       --»     £*»  f         I    -r-^""        -,  •    . 

&%$   ,.-;-'".'•  '>.:••       '.  - 

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WS   .-  *C6^          ^   ^'O.A 


*-    ^  •  .       •  -  k     •  j 

i$3     3$ 

,-\^.:^,S^: 

-'  *" 


148 


MEMOIR   NO.    1,   HUNTINGTON,   1911 


FIGURES  149  AND  150 


149  Same,   section  2. 

150  Same,  section  3. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  79 


I 


•  •  Vv-  -  3e     -     -.?~!55 

^^ 

*  *> 

-  '      '^'^^ 


149 


v*  '  •        '      -     "          y  •>,-- 


150 


MEMOIR   NO.   1,   HUNTINGTON,    1911 


FIGURES  151  AND  152 


151  Same,  section  10. 

152  Same,  section  15. 


THE  SYSTEMIC   LYMPHATIC  VESSELS 


PLATE   80 


^milifei"; 

V     V«;$L;:C  "  •  '•  Vfy^Svw  •-•': --'••'    Ji% 

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>•&•  i  •  -  -%C!-^^"  ?-^i     jR' : 

/  ^    .  is  v  /-  °  ^Z^eta-^&Z'  '.-  ?• ,  '.  8P     *'  >^i'/  .-   . 


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s* 


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?v'l    XXi, 

ssi !< 


151 


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r'f    •'     s       *r 

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152 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURE  153 
153     Same,   section  16. 

1  Sympathetic    nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Precardinal  or  precava,  resp.  azygos  of  left  side. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10  Pulmonary   artery. 

22  Vagus. 

36  Thoracic  duct,  azygos  segment. 

37  Broncho-mediastinal   duct! 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  81 


153 


MEMOIR    NO.     1,    HUNTINGTON,    1911 


FIGURE  154 

154    Transverse  section  through  ventral  portion  of  upper  thoracic  region  in 
a  20  mm.  cat  embryo  (series  241,  slide,  XIX,  section  18),  X  225. 

3  Right  precaval  vein. 

7  Aorta. 

8  Oesophagus. 

9  Trachea. 

10  Pulmonary  artery. 

18  Peritracheal  venous  plexus. 

22  Vagus. 

37  Broncho-mediastinal  duct. 


THE  SYSTEMIC  LYMPHATIC   VESSELS 


10 


154 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  155  AND  156 


155  Same,  section  19. 

156  Same,  section  20. 

3  Right  precaval  vein. 

7  Aorta. 

9  Trachea. 

10  Pulmonary  artery. 

22  Vagus. 

37  Broncho-mediastinal    duct. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  83 


37 


7 
22 


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i^il«a»j 

% 


10 


155 


9 


156 


MBMOIR   NO.    1,   HUXTIN'GTON,    1911 


FIGURES  157  AND  158 


157  Same,  section  21. 

158  Same,  section  22. 

9  Trachea. 

10  Pulmonary  artery. 

22  Vagus. 

37  Broncho-mediastinal   duct. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  84 


157 


10 


\rm 


W£$? 


22 


%&iV'^£||£;i2L 


X         •, 


* 


37 


j£%* 

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158 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


DEVELOPMENT  OF  THE  THORACIC  DUCT          107 

B.  The  development  of  the  proximal  portion  of  the  thoracic  duct 
proper,  between  the  termination  of  thoracic  duct  approach  of  the 
jugular  lymph  sac  and  the  beginning  of  the  azygos  segment  of  the 
thoracic  ducts,  caudal  to  the  leuel  of  the  aortic  arch,  viz.  the  preazy- 
gos  segment  of  the  thoracic  duct. 

In  the  earlier  purely  venous  stages  a  venous  plexus  between 
oesophagus  and  vertebral  column  (17,  fig.  101),  drains  caudo- 
laterad  into  the  mesal  surface  of  the  main  jugular  and  innomi- 
nate trunks.  This  plexus  continues  the  supracardinal  venous 
line  cephalad  beyond  the  level  of  the  azygos-Cuvierian  junc- 
tion. The  terminals  of  this  plexus  are  frequently  joined  by 
dorsal  somatic  venous  tributaries  (16,  fig.  101),  near  their  entrance 
into  the  main  vein.  These  vessels  have  been  previously  discussed 
in  their  relation  to  the  general  tributary  system  of  the  jugulo- 
innominate  line  (cf.  supra  p.  (92),  and  their  disposition  is  sche- 
matically shown  in  fig.  101. 

In  a  14  mm.  embryo  (series  210,  slide  viii,  section  41,  X  225) 
the  dorso-medial  or  pre vertebral  tributary  (17)  and  the  dorsal 
somatic  branch  (16)  are  shown  in  fig.  102,  just  prior  to  their 
union  into  the  common  large  trunk  emptying  into  the  dorso- 
medial  angle  of  the  internal  jugular  vein  (25),  dorsal  to  the  sym- 
pathetic nerve  (1). 

The  same  plexus  elements  (16  and  17)  are  seen  in  another  14 
mm.  embryo  (series  212,  slide  vii,  section  23,  X  150)  in  fig.  159. 
In  this  section  their  point  of  confluence  and  the  entrance  of  the 
resulting  combined  trunk  into  the  internal  jugular  vein  takes 
place  ventral  to  the  sympathetic  nerve  (1),  between  the  same 
and  the  left  subclavian  artery  (33),  by  utilizing  the  pathway 
afforded  by  the  peritracheal  plexus  (18,  in  fig.  102). 

Figs.  160  and  161  show  these  tributaries  (16  and  17)  in  a  13.5 
mm.  cat  embryo  (series  189,  slide  vii,  sections  20  and  21)  in  a 
magnification  of  225  diameters,  as  they  are  approaching  their 
confluence  and  point  of  entrance  into  the  internal  jugular  vein 
(25).  In  addition  these  sections  afford  admirable  examples  of 
two  other  conditions,  previously  noted  (vide  supra  pp.  49) : 

a.  The  development  of  independent  mesenchymal  intercellular 
lymphatic  spaces,  with  well  defined  endothelial  limiting  walls. 


108      DEVELOPMENT   OF   THE   SYSTEMIC    LYMPHATIC    VESSELS 

Such  spaces  (77)  are  seen  in  the  two  sections  lateral  to  the 
oesophagus.  They  apparently  develop  from  the  beginning  as 
intercellular  clefts,  without  relation  to  embryonic  veins.  The 
preazygos  region  presents  these  spaces  in  almost  all  13  and  14 
mm.  embryos.  Their  development  in  the  mammalian  embryo  is 
of  the  utmost  phylogenetic  significance  and  affords  important  evi- 
dence in  the  interpretation  of  systemic  lymphatic  ontogenesis  in 
the  sauropsida,  and  especially  in  reptiles.  The  investigation  of 
avian  and  reptilian  lymphatic  development  has  been  carried  on 
for  the  past  year  in  the  anatomical  laboratory  of  Columbia  Uni- 
versity. These  researches  are  now  nearly  completed,  and  some 
of  the  main  results  were  presented  at  the  27th  session  of  the 
American  Association  of  Anatomists  at  Cornell  University  in 
December  of  last  year.  They  establish  a  common  genetic  ground 
plan  for  the  development  and  adult  organization  of  the  amniote 
lymphatic  system.  The  avian  and  reptilian  type  only  differs 
from  that  encountered  in  the  mammal  in  respect  to  the  higher 
degree  of  development  of  the  jugular  lymph  sac,  as  an  anterior 
or  cervical  veno-lymphatic  heart,  in  the  ontogenetic  appearance 
of  other  areas  of  equal  phylogenetic  significance,  as  remnants  of  the 
multiple  ancestral  series  of  segmental  veno-lymphatic  hearts, 
and  in  the  preponderance  of  peripheral  lymphatic  development 
by  confluence  of  independent  intercellular  mesodermal  spaces, 
not  associated  topographically,  as  in  the  mammal,  with  tem- 
porary embryonic  venous  channels.  In  other  words,  the  extra- 
intimal  peri  venous  development  of  the  majority  of  peripheral 
lymphatic  channels  described  in  this  communication  appears 
as  a  caenogenetic  process  in  the  mammalian  embryo,  whereas 
in  the  sauropsid  amniotes  most  of  the  systemic  lymphatic 
channels  develop  along  more  primitive  phylogenetic  lines,  by  the 
direct  confluence  of  numerous  intercellular  mesodermal  spaces. 

These  relative  conditions  have  been  outlined  in  a  previous 
publication  on  the  phylogenetic  relations  of  the  lymphatic  and 
blood- vascular  systems  in  vertebrates.38  The  results  of  the  more 

38  Geo.    S.   Huntington,    "The   phylogenetic  relations   of  the    lymphatic  and 
blood-vascular  systems  in  vertebrates." 
Anat.  Record,  vol.  IV,  no.  1,  January  1910. 


DEVELOPMENT  OF  THE  THORACIC  DUCT          109 

recent  detailed  investigations  of  lymphatic  development  in  birds 
and  reptiles  have  fully  sustained  the  interpretation  given  in  the 
publication  quoted. 

b.  The  darkly  stained  mass  of  cells  seen  in  the  interval  between 
16  and  17  in  both  sections  is  the  result  of  obliteration  of  early 
embryonic  vascular  channels,  which  have  lost  their  connection 
with  the  vessels,  and  whose  endothelial  walls  are  apparently  in 
the  process  of  reverting  to  indifferent  mesodermal  cells.  Many 
of  these  degenerated  vascular  aggregations  are  formed  in  embryos 
between  13  and  15  mm.  crown-rump  measure. 

Some  of  the  elements  of  this  early  embryonic  prevertebral 
venous  plexus  are  secondarily  replaced  by  perivenous  or  extrainti- 
mal  lymphatic  spaces  in  exactly  the  same  way  as  is  observed  in 
the  development  of  the  ventral  mediastinal  duct.  The  resulting, 
originally  separate,  extraintimal  lymphatic  anlages,  having  re- 
placed the  venule  along  and  around  which-  they  primarily  devel- 
oped, unite  with  each  other  and  form  the  preazygos  segment 
of  the  thoracic  duct,  between  the  thoracic  duct  approach  of  the 
jugular  lymph  sac  and  the  level  of  the  aortic  arch,  at  which  the 
azygos  portion  of  the  thoracic  duct  begins. 

Fig.  162  shows  a  transverse  section  of  the  left  side  of  the  upper 
thoracic  region  in  a  14  mm.  cat  embryo  (series  210,  slide  IX, 
section  26,  X  200).  The  prevertebral  tributary  plexus  (17)  turns 
mesad  of  the  sympathetic  nerve  (1)  to  enter  the  dorso-medial 
angle  of  the  left  innominate  vein  (40).  Dorsad  of  the  main  vein 
is  the  ascending  portion  of  the  left  subclavian  artery  (33).  Be- 
tween aorta  (7)  and  innominate  vein  (40)  are 'other  elements  of 
the  mediastinal  venous  plexus,  in  the  interval  between  the  sympa- 
thetic nerve  (1)  and  the  vagus  (22),  with  ventral  branches  (32)  in 
front  of  the  latter. 

Between  the  oesophagus  and  the  prevertebral  plexus  (17)  is 
an  area  in  which  venous  elements  (4),  formerly  connected  with 
the  same,  are  undergoing  replacement  by  the  extraintimal  lym- 
phatic anlages  (5)  of  the  preazygos  segment  of  the  thoracic  duct. 
These  structures  cannot  be  distinctly  made  out  in  fig.  162,  but 
they  are  shown  in  a  higher  magnification  in  detail  in  fig.  163, 
which  includes  the  region  of  the  same  section  dorsal  to  the  oesoph- 


110       DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

agus  magnified  225  diameters.  The  prevertebral  venous  plexus 
(17)  extends  in  an  arch  concentric  with  the  dorsal  circumference 
of  the  oesophagus  (8),  in  front  of  the  vertebral  centers.  Between 
it  and  the  oesophagus,  mesal  to  the  sympathetics  (1),  are  seen 
on  each  side  former  elements  of  the  venous  plexus  (4)  surrounded 
by  the  extraintimal  lymphatic  anlages  (5)  of  the  preazygos  seg- 
ment of  the  thoracic  duct. 

Figs.  164,  165  and  166  show  the  same  structures  in  the  next 
three  sections  (25,  24  and  23),  proceeding  cephalad.  Fig.  166 
is  especially  clear.  In  it  the  original  line  of  connection  of  the 
atrophying  venous  kernel  (4)  with  the  prevertebral  plexus  (17) 
can  still  be  made  out  as  a  band  of  condensed  mesoderm,  and 
the  endothelium  of  the  perivenous  lymphatic  space  (5)  is  clearly 
marked. 

Figs.  167  and  168  show  this  area  in  two  successive  sections  of 
the  same  embryo  further  caudad  (series  210,  slide  ix,  sections 
43  and  44,  X  150),  and  fig.  169  gives  the  last  section  magnified 
200  diameters.  The  empty  central  venous  remnant  (4),  with 
the  enveloping  extraintimal  lymphatic  anlage  (5),  and  the  still 
functional  elements  of  the  prevertebral  plexus  (17),  can  be  seen 
in  all  of  the  sections.  They  also  show,  nearer  to  the  dorso- 
lateral  wall  of  the  oesophagus,  one  of  the  collections  of  darkly 
stained  mesodermal  cells  above  referred  to  as  representing  rem- 
nants of  formerly  patent  blood-vessels. 

The  series  of  microphotographs  shown  in  figs.  160  to  169 
inclusive  again  conclusively  demonstrates  the  origin  of  this 
portion  of  the  lymphatic  channel  by  confluence  of  independent 
extraintimal  mesenchymal  spaces  surrounding  and  replacing 
degenerating  embryonic  venules.  The  reproductions  only  give 
relatively  faint  and  indistinct  views  of  the  actual  conditions  ob- 
served under  the  microscope.  The  general  mesenchymal  tissue 
in  this  region  is  extremely  loose  and  the  area  is  very  difficult 
to  photograph  sharply  and  distinctly.  The  actual  sections, 
however,  offer  histological  pictures  identical  with  those  observed 
as  above  described  in  the  development  of  the  ventral  mediastinal 
lymphatic  duct.  The  extraintimal  lymphatic  spaces  are  either 
closely  applied  to  part  of  the  circumference  of  the  wall  of  the 


DEVELOPMENT  OF  THE  THORACIC  DUCT          111 

shrinking  venule,  or  they  occasionally  completely  surround  the 
same.  In  the  former  case  the  contained  venous  remnant  is 
connected  at  part  of  its  periphery  with  the  wall  of  the  envel- 
oping lymphatic  space.  In  the  latter  and  more  exceptional  case, 
the  free  ventral  nucleus  of  the  lymphatic  space  is  formed  by  the 
atrophied  vein.  In  either  case  the  lumen  of  the  latter  may  con- 
tain a  few  degenerated  red  blood  cells.  These  pictures  are  again 
constant  in  embryos  of  the  appropriate  stages.  The  lymphatic 
anlage  can  be  accurately  traced  from  its  indefinite  beginning 
among  the  perivenous  mesenchymal  intercellular  clefts  through 
a  number  of  successive  sections  to  its  similar  distal  terminations 
in  the  same  intercellular  plexus.  Following  the  sections  from 
this  point  caudad  through  a  varying  intervening  area  in  which 
no  distinct  lymphatic  channel  appears,  the  same  line  will  sooner 
or  later  reveal  the  repetition  of  the  same  process,  and  the  formation 
of  another  link  in  the  still  disjointed  chain  of  primitive  lymphatic 
anlages. 

It  is  again  to  be  noted  here  that  in  the  earlier  stages  (13,  13.5, 

14  mm.),  the  individual  spaces,  plus  their  kernel  of  atrophied 
vein,  are  relatively  larger  than  in  the  later  (15-15.5  mm.)  em- 
bryos.    In  the  earlier  stages  (13  mm.,   13.5  mm.  and  14  mm. 
embryos)  these  separate  and  still  isolated  segments  of  the  future 
continuous  lymphatic  channel  begin  and  end  blindly.     In  the 

15  and  15.5  mm.  stages  they  have  increased  in  number  and  ad- 
jacent links  have  united  to  form  longer  segments.     Finally,  in 
the  16  mm.  cat  embryo,  the  preazygos  portion  of  the  thoracic 
duct  is  usually  established  as  a  nearly  continuous  channel  through 
the   further   confluence   of  the   originally  separate  and  distinct 
components.     Every  stage  of  the  extraintimal  lymphatic  develop- 
ment can  be  observed  with  absolute  certainty  and  accuracy  in 
every  series  within  the  proper  length  limits. 


PART  II,  PLATES 

FIGURES  159  TO  169 


FIGURE  159 

159     Transection  of  upper  thoracic  region  in  a  14  mm.  cat  embryo  (series  212, 
slide  VII,  section  23),  X  150. 


1  Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

11  Jugular  lymph  sac. 

16  Dorso-medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus. 

20  Subthymic  venous  plexus. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 
25  Internal  jugular  vein. 
33  Left  subclavian  artery. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  85 


16 


20- 


159 


MKMOIR    NC).    1,    HUNTINOTON,    1911 


FIGURES  160  AND  161 

160  Transverse  section  of  dorsal  portion  of  upper  thoracic  region  in  a  13.5  cat 
embryo  (series  189,  slide  VII,  section  20),  X  225. 

161  Same,  section  21. 

1  Sympathetic  nerve. 

16  Dorso-medial  somatic  venous  tributaries. 

17  Prevertebral  venous  plexus. 
22.  Vagus. 

25     Internal  jugular  vein. 

77     Mesenchymal   intercellular   lymphatic   anlages. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE 


17 


W^^&^KI 
m^r&^m^r 


22 


161 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


162  Transverse  section  of  upper   thoracic  region   in  a  14  mm.  cat    embryo 
(series  210,  slide  IX,  section  26),  X  200. 

163  Dorsal   portion   of   same   section,  X  225. 

1     Sympathetic  nerve. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of   develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or   perivenous  lymphatic  space  surrounding   degen- 

erating embryonal  vein. 

7  Aorta. 

17  Prevertebral  venous  plexus. 

22  Vagus. 

32  Ventral  mediastinal  venous  plexus. 

33  Left  subclavian  artery. 
40  Innominate  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE     S7 


32 


162 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  164,    165  AND  166 

164  Same,  section  25. 

165  Same,  section  24. 

166  Same,  section  23.     . 

1     Sympathetic  nerve. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or    perivenous    lymphatic    space  surrounding    degen- 

erating embryonal  vein. 
8     Oesophagus. 
17     Prevertebral  venous  plexus. 


]7 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE 


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i.  «« *v    .  •««        vJT/«   .\-r  «aP^    ^JELrjih-K^r  ?*  '     .*».*. 


166 


MKMOIH    NO.    1,   HUNTINGTON,    1911 


FIGURES  167  AND  1H8 

167  Same,   section  43  X  150. 

168  Same,   section  44  X  150. 

1     Sympathetic  nerve. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of    develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space    surrounding    degen- 

erating embryonal  vein. 
17     Prevertebral  venous  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE 


S**/'* '    * "   '"•***•"  ''^^y'^l^''^""^^^^  * VV'^K  *'  'v 


v  » 

•^ 


168 


MEMOin   NO.   1,  HUNTINGTON,    1911 


FIGURE  169 

169     Same,   section  44.     X  200. 

1     Sympathetic  nerve. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic   space  surrounding  degener- 

ating embryonal  vein. 
8    Oesophagus. 
40     Innominate  vein. 


THE   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE  «M> 


169 


MK.MOIH   NO.    1,   HUNTINGTON,    1911 


DEVELOPMENT    OF   THE    SYSTEMIC    LYMPHATIC    VESSELS       113 

C.  The  junction  of  the  two  independently  formed  lymphatic  chan- 
nels above  described,  viz.,  the  preazygos  segment  of  the  thoracic  duct 
and  the  ventral  mediastinal  trunk,  with  each  other  and  with  the  tho- 
racic duct  approach  of  the  jugular  lymph  sac. 

In  the  15  and  15.5  mm.  embryo  of  the  cat  the  thoracic  duct 
approach  of  the  jugular  lymph  sac  has  extended  mesad  between 
the  common  jugular  and  innominate  veins  and  the  thyro-cervical 
or  subclavian  arteries  to  the  interval  between  the  main  vein  and 
the  sympathetic  nerve.  In  this  region  the  process  makes  second- 
ary connections  with  the  independently  developed  ventral  medias- 
tinal lymphatic  trunk  and  with  the  equally  independently  formed 
preaortic  segment  of  the  thoracic  duct. 

The  order  of  this  union,  as  previously  explained,  appears  to 
have  an  important  influence  on  the  subsequent  topographical 
position  of  this  portion  of  the  adult  thoracic  duct.  If  the  jugular 
sac  approach  first  meets  and  unites  with  the  ventral  mediastinal 
lymphatic  channel,  then  the  entire  duct  appears  to  pass  ventrad  to 
the  sympathetic  strand,  between  it  and  the  adjacent  dorso-medial 
surface  of  the  main  vein,  to  turn  subsequently  dorsad  towards  the 
pre vertebral  region  on  the  mesal  aspect  of  the  nerve  (reconstruc- 
tion, fig.  171,  series  143,  slides  x  and  xi,  figs.  172  to  183). 

If,  on  the  other  hand,  the  thoracic  duct  approach  first  joins 
the  preazygos  segment  of  the  thoracic  duct,  developed  by  the 
confluence  of  the  dorsal  perivenous  lymphatic  anlages  accom- 
panying and  surrounding  the  prevertebral  venous  plexus  cephalad 
of  the  aortic  arch  level,  then  the  resulting  thoracic  duct  passes 
dorso-laterad  to  the  sympathetic  nerve,  after  having  received 
the  ventral  mediastinal  trunk  through  the  interval  between  this 
nerve  and  the  main  vein  (text  figs.,  p.  (72). 

Fig.  170  shows  in  a  dorsal  view  the  reconstruction  of  the  left 
vascular  complex  of  the  lower  cervical  and  upper  thoracic  regions 
in  a  15  mm.  cat  embryo  (series  218,  slides  VIII,  sections  25^44; 
ix,  sections  1-48;  x,  sections  1-48;  xi,  sections  1-48;  xii, 
sections  1-48.) 

The  reconstruction  should  be  followed  in  the  direction  caudo- 
cephalad.  The  caudal  part  of  the  reconstruction  includes 


114  DEVELOPMENT    OF    THE     THORACIC     DUCT 

the  cephalic  portion  of  the  azygos  system.  The  left  (6")  and 
the  right  (3f)  azygos  veins  are  seen  arching  caudo-cephalad  to 
empty  into  the  left  (6)  and  right  (5)  precavae.  They  are  joined 
by  the  broad  plexiform  plate  of  the  interazygos  anastomosis, 
whose  meshes  are  perforated  by  the  intersegmental  arteries.  The 
sympathetic  nerve  strands  (1)  lie  between  the  arterial  branches 
and  the  azygos  trunks,  in  the  a  gle  between  them  and  their 
dorsal  somatic  tributaries.  Ventro-mesad  of  the  right  precava 
(3)  is  seen  the  right  vagus  (22).  The  distal  end  of  the  right  pul- 
monary artery  (10)  is  seen  below  the  right  azygos-caval  arch 
(3'-3),  surrounded  by  the  channel  of  the  broncho-mediastinal 
trunk  (37).  In  the  azygos-caval  arch,  and  along  the  right  pre- 
cava (3)  are  the  precaval  lymphatic  anlages  (53}  previously 
referred  to  (cf.  supra  pp.  (30)  as  being  the  first  extraintimal 
lymphatic  spaces  to  develop  in  this  region,  as  early  as  the  12 
mm.  stage  (cf.  figs.  TO  and  11. 

The  cephalic  portion  of  the  azygos  segment  of  the  thoracic 
duct,  well  developed  in  this  stage,  is  hidden  in  this  view  of  the 
reconstruction  by  the  dorsal  interazygos  venous  plexus,  on  the 
ventral  face  of  which  the  lymphatic  network  is  situated.  Only 
a  few  scattered  and  isolated  lymphatic  anlages  are  seen  projecting 
cephalad  of  this  anastomosis,  and  not  yet  joined  to  the  preazygos 
segment  of  the  thoracic  duct  (35). 

Cephalad  of  the  area  just  described  are  the  large  arterial  ves- 
sels, viz.,  the  Ductus  arteriosus  Botalli  (56),  the  aortic  arch  (7), 
the  right  subclavian  artery  (57),  the  innominate  continuation  of 
the  carotid  trunk  (45),  and  the  left  subclavian  artery  (33),  with 
the  left  vertebral  (41)  and  thyro-cervical  (24)  arteries  arising 
from  it.  The  ventrolateral  continuation  of  the  left  subclavian 
cannot  be  seen  in  this  view  of  the  reconstruction.  Ventrad  of 
the  thoracic  aorta  is  seen  the  ventral  mediastinal  venous  plexus 
with  the  accompanying  cephalic  part  of  the  broncho-mediastinal 
lymphatic  complex  (upper  37  in  fig.  170). 

The  preazygos  segment  of  the  thoracic  duct  (35)  appears  as  a 
well  developed  channel  on  the  dorso-medial  aspect  "of  the  aortic 
arch,  ascending  behind  the  left  subclavian  artery  (33).  A  number 
of  scattered  lymphatic  anlages,  at  the  level  of  leader  35,  offer 


DEVELOPMENT    OF  THE  SYSTEMIC    LYMPHATIC    VESSELS       115 

the  genetic  opportunity  of  establishing,  in  later  stages,  a  communi- 
cation between  the  preazygos  thoracic  duct  (35}  and  the  broncho- 
mediastinal  channel  (37),  which  would  correspond  to  the  distal 
connection  noted  above  (cf.  p.  (85) in  the  adult  between  these  two 
lymphatic  channels  (cf.  figs.  94,  95,  96  and  97). 

The  cephalic  end  of  the  preazygos  segment  of  the  thoracic  duct 
still  ends  blindly  in  this  stage  in  two  longer  prolongations,  the 
connection  with  the  thoracic  duct  approach  of  the  jugular  lymph 
sac  not  having  been  as  yet  established.  The  latter  rides  in  the 
fork  between  the  main  jugular  vein  and  the  entrance  of  the  left 
superior  intercostal  vein  (16-46).  One  process  of  the  approach 
(12)  hooks  caudad  on  the  dorso-lateral  side  of  this  vein,  between  it 
and  the  thyrocervical  artery  (24)  and  ends  blindly  lateral  to  the 
sympathetic  nerve  (/).  Another  blunt  terminal  of  the  thoracic 
duct  approach  turns  ventro-mesad,  between  vagus  (22)  and  sym- 
pathetic nerve  (1),  and  is  exposed  in  the  reconstruction  by  the 
removal  of  a  segment  of  the  latter  nerve  which  otherwise  would 
hide  it  in  the  dorsal  view  here  given.  A  long  slender  process  passes 
from  this  portion  of  the  thoracic  duct  approach  ventro-mesad 
between  the  vagus  (22)  and  carotid  (22).  This  process,  which 
seems  to  be  constantly  present,  probably  effects  in  later  stages  a 
connection  with  the  cephalic  part  of  the  ventral  mediastinal  lym- 
phatic plexus. 

It  is  evident,  in  considering  the  detached  and  isolated  lym- 
phatic anlages  intervening  here  between  the  thoracic  duct  approach 
and  the  blind  cephalic  end  if  the  preazygos  segment  of  the  thoracic 
duct  already  formed  (35}  that  in  course  of  further  development  the 
union  between  the  latter  and  the  jugular  sac  could  have  been  es- 
tablished either  on  the  dorso-lateral  or  ventro-medial  side  of  the 
sympathetic  nerve,  thus  leading  to  one  or  the  other  of  the  topo- 
graphical conditions  above  discussed  (cf .  p.  75  and  text  figures) . 

The  fifth  spinal  nerve  (54)  still  penetrates  the  caudo-lateral 
part  of  the  lymph  sac.  Below  the  same  are  seen  the  sixth,  seventh 
and  eight  segmental  nerves  of  the  brachial  plexus  (55) .  The  thyro- 
cervical artery  (24)  sends  its  ventral  branch  forward  between  the 
jugular  and  subclavian  approaches  of  the  lymph  sac  (just  caudal 
to  vein  16-46),  and  then  continues  cephalad  on  the  doral  aspect  of 
the  sac. 


116          DEVELOPMENT  OF  THE  THORACIC  DUCT 

Fig.  171  shows  a  reconstruction  of  the  left  vascular  complex  of 
the  lower  cervical  and  upper  thoracic  regions  in  a  15.5  mm.  cat 
embryo  (series  143,  slides  viii,  ix,  x,  xi,  and  xii,  225)  viewed 
from  the  right  side  and  from  behind,  and  figs.  172  to  183 
give  transverse  sections  of  the  left  upper  thoracic  region  in  the 
same  embryo,  selected  from  slides  xi  and  x.  The  figure  of  the 
reconstruction  gives  by  means  of  side  lines  and  roman  numerals 
the  level  of  the  slides  entering  into  its  composition,  so  that  the 
individual  sections  shown  in  the  microphotographs  can  be  referred 
to  and  oriented  by  the  reconstruction. 

The  reconstruction  as  well  as  the  photographs  of  the  sections 
should  be  followed  from  below  upwards. 

Description  of  reconstruction,  fig.  171.  The  reconstruction  is 
carried  caudad  to  the  upper  azygos  region.  The  right  azygos 
arch  (3'}  is  seen  entering  the  dorsal  circumference  of  the  right 
precava  (3).  Azygos  (6')  and  precava  (6)  of  the  left  side  cannot 
be  distinctly  seen  in  this  view  of  the  model.  Mesal  to  the  right 
praecava  (3)  is  the  right  vagus  (22). 

Projecting  cephalad  above  the  azygos  arches  and  the  interazy- 
gos  anastomosis  are  seen  the  cephalic  elements  of  the  azygos  por- 
tion of  the  thoracic  ducts  (36),  which  extend  thence  caudad  along 
the  ventral  surface  of  the  azygos  complex.  The  cephalic  end  of 
the  azygos  segment  of  the  ducts  has  not  yet  joined  the  caudal 
extremity  of  the  preazygos  segment  (35),  although  they  have 
approached  each  other  closely,  and  adjacent  detached  lymphatic 
elements  between  them  foreshadow  their  coming  union. 

The  preazygos  segment  of  the  thoracic  duct  (35)  is  a  well  devel- 
oped plexiform  channel,  which  receives  a  considerable  branch 
from  the  lymphatic  complex  along  the  ventral  aspect  of  the  pre- 
vertebral  venous  plexus  (.77).  The  latter  is  now  fully  formed  and 
differentiated  clearly  from  the  adjacent  lymphatics,  draining  as 
a  chain  of  venous  spaces  caudad  into  the  azygos  arches.  This 
central  part  of  the  preazygos  duct  (35)  intersects  with  the  medial 
aspect  of  the  large  vertebral  vessels  (41,  4%)  and  the  underlying 
left  subclavian  artery  and  receives  just  caudal  to  this  point  a 
lymphatic  channel  connecting  it  with  the  broncho-mediastinal 
duct.  This  lymphatic  vessel  cannot  be  seen  distinctly  in  this 


DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS       117 

view  of  the  reconstruction,  because  it  is  largely  under  cover  of  the 
extensive  venous  plexus  encrusting  the  medial  surface  of  the 
left  innominate  vein  on  which  it  lies.  It  can,  however,  be  clearly 
traced  in  the  corresponding  sections  of  slides  xi  and  x  shown  in 
figs  172  to  183  (cf.  infra). 

The  preazygos  segment  of  the  thoracic  duct  then  continues  on 
the  mesal  side  of  the  sympathetic  (1}  cephalad,  swings  laterad  on 
the  ventrolateral  aspect  of  the  nerve,  between  it  and  the  common 
jugular  vein,  mesal  to  the  thyrocervical  artery  (24),  and  unites 
in  this  situation  with  the  thoracic  duct  approach  of  the  jugular 
lymph  sac  (12).  The  latter  extends  as  a  well  defined  prolongation 
from  the  dorsal  aspect  of  the  jugular  approach  (13). 

The  aortic  arch  (7)  with  the  innominate  trunk  (45),  the  right 
subclavian  origin  (57)  and  the  two  carotid  arteries  (23,  32'), 
occupies  the  centre  of  the  model.  The  left  subclavian  artery 
cannot  be  followed  in  this  view,  but  the  left  vertebral  artery  (41) 
is  shown.  Further  ventrad  is  the  section  of  the  left  innominate 
vein  (40).  The  thymus  (21}  is  nearly  buried  in  the  extensive 
perithymic  venous  anastomosis  (19,  20},  which  also  hides  from 
view  the  most  of  broncho-mediastinal  lymphatic  plexus. 

The  thyrocervical  artery  (24)  perforates  between  the  two  divi- 
sions of  the  lymph  sac,  lateral  to  the  jugular  approach  (13).  The 
fifth  spinal  nerve  (54)  and  a  companion  vein  still  penetrate  the 
caudo-lateral  part  of  the  sac.  Further  caudad  and  laterad  are  the 
sixth  and  seventh  segmental  nerves  (55).  The  jugular  approach 
sends  a  caudal  prolongation  along  the  dorse-medial  aspect  of  the 
main  vein,  between  it  and  the  sympathetic  nerve,  which  parallels 
the  thoracic  duct  approach,  and  may,  together  with  a  large  de- 
tached lymphatic  island  further  caudad,  represent  an  incomplete 
form  of  double  or  bifid  thoracic  duct  approach  as  previously 
described  (cf.  supra,  p.  63,  text  figure.) 

Union  of  broncho-mediastinal  duct  with  preaortic  portion  of  thor- 
acic duct  and  junction  of  both  with  thoracic  duct  approach  of  the 
jugular  lymph  sac.  The  achievement  of  this  stage  is  excellently 
illustrated  in  the  microphotographs  of  this  15.5  mm.  embryo 
(series  143)  shown  in  figs.  172  to  183.  In  fig.  172  (series  143,  slide 
xi,  section  16),  a  section  through  the  left  side  of  the  upper  thoracic 


118          DEVELOPMENT  OF  THE  THORACIC  DUCT 

region,  the  cephalic  end  of  the  preaortic  segment  of  the  thoracic 
duct  (fig.  172,  35}  is  seen  lateral  to  the  oesophagus  (8],  between 
the  sympathetic  nerve  (1)  dorsad  and  the  subclavian  artery  (33) 
and  left  innominate  vein  (40)  ventrad.  The  cephalic  end  of  the 
broncho-mediastinal  channel  (37)  lies  in  the  angle  between  sub- 
clavian artery  and  innominate  vein,  lateral  to  and  at  some  dis- 
tance from  the  trachea  (9).  The  two  lymphatic  channels  are 
traced  in  the  succeeding  sections  cephalad  to  their  union  and  their 
continuation  with  the  thoracic  duct  approach  of  the  jugular 
lymph  sac. 

In  fig.  173  (series  143,  slide  xi,  section  14)  the  lymphatic  ducts 
have  approached  each  other  and  a  third  lymphatic  cross-section 
appears  mesal  to  the  subclavian  artery  in  the  interval  between  the 
thoracic  duct  and  the  broncho-mediastinal  channel,  foreshadow- 
ing their  approaching  fusion  (38).  In  fig.  174  (series  143,  slide  xi, 
section  12)  this  fusion  has  occurred  (38  in  fig.  174  representing 
union  of  35  and  37) 

In  fig.  175  (series  143,  slide  xi,  section  11)  the  connection  is 
interrupted,  and  in  the  succeeding  sections  (figs.  176,  177, 178  and 
179)  the  two  components  of  the  area  of  confluence  (38),  viz,  the 
preaortic  thoracic  duct  segment  and  the  broncho-mediastinal 
trunk,  remain  separated  from  each  other.  The  latter  assumes  more 
and  more  the  typical  character  of  the  thoracic  duct  approach  of 
the  jugular  lymph  sac,  as  previously  described  (cf.  p.  60), 
occupying  the  typical  neuro-venous  recess  between  sympathetic 
nerve  and  innominate  vein,  as  shown  well  in  figs.  178  and  179 
(series  143,  slide  xi,  section  2,  and  slide  x,  section  32). 

In  fig.  180  (series  143,  slide  q,  section  28)  the  two  lymphatic 
components  have  again  united  (38),  and  they  continue  from  this 
point  on  as  a  single  channel  following  the  typical  course  of  the 
thoracic  duct  approach  of  the  jugular  lymph  sac  cephalad  to  union 
with  that  structure. 

We  have  therefore  in  this  stage  a  gradual  approach  of  the  cepha- 
lic ends  of  the  preaortic  segment  of  the  thoracic  duct  and  of  the 
ventral  broncho-mediastinal  trunk,  a  preliminary  anastomosis 
between  them  (figs.  173,  174),  followed  further  cephalad  by  a 
final  confluence  and  union  with  the  thoracic  duct  approach  of  the 
jugular  lymph  sac. 


DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS          119 

A  comparison  of  the  series  just  studied  (series  143)  with  another 
15.5  mm.  embryo  (series  141)  shows  identical  conditions.  Thus 
figs.  184  and  185  show  transverse  sections  through  the  upper  part 
of  the  left  thoracic  region  of  the  embryo.  In  fig.  184  the  preazy- 
gos  segment  of  the  thoracic  duct  and  the  broncho-mediastinal 
trunk  (38)  are  approaching  each  other  in  the  interval  between  the 
innominate  vein  (50)  and  the  subclavian  artery  (33)  laterad,  and 
trachea  (9)  and  oesophagus  (8)  mesad.  This  quite  agrees  with 
the  conditions  seen  in  series  143,  in  figures  172  amd  173  (sections 
16  and  14  of  slide  xi).  In  fig.  185  (slide  x,  section  21  of  series 
141)  the  two  lymphatic  anlages  have  joined  (38),  repeating  practi- 
cally conditions  which  series  143  shows  in  sections  11  and  12  of 
slide  xi,  figs.  174  and  175.  The  permanent  functional  peri- 
tracheal  venous  plexus  (18)  appears  clearly  differentiated  from  the 
lymphatic  channels  in  both  sections. 

The  earlier  stages  in  the  development  of  this  junctional  area 
just  studied  in  the  15.5  mm.  stages  (series  143  and  141)  are  found 
in  a  13.5  mm.  cat  embryo,  series  223.  Two  sections  of  the  left  upper 
thoracic  region  are  shown  in  figs.  186  and  187  (series  223,  slide 
viii,  sections  39  and  40,  X  225).  The  sections  pass  through  the 
left  innominate  vein  (40),  the  left  subclavian  artery  (33),  at  the 
level  of  origin  of  the  vertebral  (41)  and  the  costocervical  arteries 
(43),  and  the  innominate  artery  (45). 

Both  sections  show  the  radicles  of  the  peritracheal  mediastinal 
venous  plexus,  and  the  beginning  replacement  of  certain  elements 
of  the  same  (4)  by  extraintimal  perivenous  lymphatic  spaces  (5), 
which  form  the  anlage  of  the  future  junctional  channel  between  the 
broncho-mediastinal  lymphatic  trunk  and  the  preazygos  segment 
of  the  thoracic  duct.  These  spaces  are  situated  dorsad  to  the  aorta 
and  the  innominate  artery  (45),  in  the  interval  between  the  tra- 
chea (9)  mesad,  the  oesophagus  (8)  dorso-mesad,  and  the  inno- 
minate vein  (40)  and  sympathetic  nerve  (1)  laterad. 

The  developing  perivenous  lymphatic  spaces  seen  here  in  this 
earlier  13.5  mm.  embryo  correspond  to  the  finished  lymphatic 
channel  segments  of  the  later  15.5  mm.  stages,  in  which  the  pre- 
azygos segment  of  the  thoracic  duct  meets  and  joins  witht  he  inde- 
pendently developed  broncho-mediastinal  trunk,  as  just  seen  in 
series  143  and  141  (figs.  172  to  185). 


PART  II,  PLATES 

FIGURES  170  TO  187 


FIGURE  170 

170  Reconstruction  of  left  vascular  complex  of  lower  cervical  and  upper 
thoracic  regions  of  a  15  mm.  cat  embryo  (series  218,  slide  VIII,  sections  25  to 
44;  slide  IX,  sections  1  to  48;  slide  X,  sections  1  to  48;  slide  XI,  sections  1  to 
48;  slide  XII,  sections  1  to  48,  X  225),  dorsal  view. 

1  Sympathetic  nerve. 

3'  Right  azygos  vein. 

3  Right  precava. 

6  Left  precava. 

6'  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

10  Pulmonary  artery. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

16  Dorso-medial  somatic  venous  tributaries. 

22  Vagus. 

24  Thyrocervical  artery. 

33  Left  subclavian  artery. 

35  Thoracic  duct,  preazygos  segment. 

35'  Detached  lymphatic  space  in  path  of  preazygos  channel. 

37  Broncho-mediastinal  duct. 

41  Vertebral  artery. 

42  Vertebral  vein. 

45  Innominate  artery. 

46  Left  superior  intercostal  vein. 

53  Precaval  lymphatics. 

54  Fifth  spinal  nerve. 

55  Sixth,   seventh  and  eighth   spinal   nerve 

56  Ductus  arteriosus  Botalli. 

57  Right  subclavian  artery. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 
16  46 


PLATE  91 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


10 


170 


FIGURE  171 

171  Reconstruction  of  left  vascular  complex  of  lower  cervical  and  upper  thoracic 
regions  in  a  15.5  mm.  cat  embryo,  (series  143,  slides  VIII,  IX,  X,  and  XI),  X  225 
View  from  behind  and  from  right  side. 

1  Sympathetic  nerve. 
3'  Right  azygos  arch. 
3  Right  precava. 

6  Left  precava. 

6'  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

13  Jugular  lymph  sac,  jugular  approach. 
17    Prevertebral  venous  plexus. 

19  Suprathymic  venous  plexus. 

20  Subthymic  venous  plexus. 

21  Thymus. 

22  Vagus. 

23  Left  carotid  artery. 
23'  Right  carotid  artery. 

24  Thyrocervical  artery. 

29    Jugulo-subclavian  trunk. 

35  Thoracic  duct,  preazygos  segment. 

36  Thoracic  duct,  azygos  segment . 

40  Innominate  vein. 

41  Vertebral   artery. 

42  Vertebral    vein. 

45  Innominate  artery. 

54  Fifth  spinal  nerve. 

55  Sixth,  seventh  and  eighth  spinal  nerve 
57  Right  subclavian  artery. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE   92 


VIII. 


XII 


171 


MEMOIR  NO.    1,   HUNTINGTON,    1911 


FIGURES  172  AND  173 

172  Transverse  section  of  left    side  of  upper  thoracic   region  of  a   15  mm. 
cat  embryo,  (series  143,  slide  XI,  section  16),  X  200. 

173  Same,  section  14. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

17  Prevertebral  venous  plexus. 

33  Left   subclavian   artery. 

35  Thoracic  duct,  preazygos  segment. 

37  Broncho-mediastinal  duct. 

38  Confluence  of  broncho-mediastinal  duct  and  preazygos  segment  of 

thoracic  duct. 
40     Innominate  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  93 


*  *  V- '.  *•  •  * Vs  (    T  ?<^4-»     v  w'-fclti 

'       -^i  '  -i>.fc<^^*^v-*     ^-V-i5*-^    '-* 


172 


.-***  -*- 

-"'-     '      • 


173 


MEMOIR  NO.   1,   HUNTINGTON,   1911 


FIGURES  174,  175  AND  176 

174  Same,  section  12. 

175  Same,  section  11. 

176  Same,  section  6. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

33  Left  subclavian  artery. 

35  Thoracic  duct,  preazygos  segment. 

37  Broncho-mediastinal   duct. 

38  Confluence  of  broncho-mediastinal  duct  and  preazygos  segment  of 

thoracic  duct. 
40     Innominate  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  94 


40 


175 


wW  <  r\\ -£>*>*• 


176 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  177,  178  AND  179 

177  Same,  section  5. 

178  Same,  section  2. 

179  Same,  slide  IX,  section  32. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

35    Thoracic  duct,  preazygos  segment. 

37  Broncho-mediastinal  duct. 

38  Confluence  of  broncho-mediastinal  duct  and  preazygos  segment  of 

thoracic  duct. 

40  Innominate  vein. 

41  Vertebral  artery. 
44     Costo-cervical  vein. 


THE  SYSTEMIC   LYMPHATIC  VESSELS 


PLATE  95 


177 


178 


40 


179 


MEMOIR   NO.    I,    HUNTINGTON      1911 


FIGURES  180,  181  AND  182 

180  Same,  slide  X,  section  28. 

181  Same,  slide  X,  section  26. 

182  Same,  slide  X,  section  23. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

33    Left  subclavian  artery. 

38    Confluence  of  broncho-mediastinal  duct  and  preazygos  segment  of 
thoracic  duct. 

40  Innominate  vein. 

41  Vertebral  artery. 

43  Costo-cervical  artery. 

44  Costo-cervical    vein. 


THE  SYSTEMIC    LYMPHATIC:   VESSELS 


PLATE   !)0 


40 


180 


181 


182 


MEMOIR   NO.   1,  HUNTINGTON,    1911 


FIGURE  183 
183    Same,  slide  X,  section  22. 

1  Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

12  Jugular  lymph  sac,  thoracic  duct  approach. 

22  Vagus. 

23  Left  carotid  artery. 

33  Left  subclavian  artery. 

35  Thoracic  duct,  preazygos  segment. 

40  Innominate  vein. 

41  Vertebral  artery. 

43  Costo-cervical  artery. 

45  Innominate  artery. 


THE    SYSTEMIC   LYMPHATIC  VESSELS 


PLATE   97 


jfr..Vfri  fojr^'j 
-  F^v^rTTrrvTpv 

al*Vr«v»Jf  T  j  **•  4»' 
x          .-  7«.v.  :•**/!  -"M     lf^. 


*  -  -  *,      '•*.     i^«  I '-  *&i 

t  v>»/*  -      *y"J  *»*»;V\i 


183 


MEMOIR  NO.   I,  HUNTINQTON,   1911 


FIGURES  184  AND  185 

184  Transverse   section    through    upper    part    of    left    thoracic  region   in   a 
15.5  mm.  cat  embryo,  (series  141,  slide  X,  section  18),  X  200. 

185  Same,   section   21. 

1     Sympathetic  nerve. 

8  Oesophagus. 

9  Trachea. 

16  Dorso-medial  somatic  venous  tributaries. 

18  Peritracheal  venous  plexus. 

22  Vagus. 

23  Left  carotid  artery. 

33     Left  subclavian  artery. 

38     Confluence  of  broncho-mediastinal  duct  and  preazygos  segment  of 

thoracic  duct. 
40     Innominate  vein. 


TI1K  SYSTKMIC  LYMPHATIC  V10SSKLS 


PLATK  98 


38 


18 


184 


^  " "     "  n 


:&jjj$$PK:  %  i  gp5  - ;.  f^'/: 


185 


MEMOIR   NO.    1,    HUNTTNGTON,    1911 


FIGURES  186  AND  187 

186  Transverse    section   of    left    upper   thoracic   region    in    a  13.5   mm.  cat 
embryo,  (series  223,  slide  VIII,  section  39),  X  225. 

187  Same,  section  40. 

1     Sympathetic    nerve. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

8  Oesophagus. 

9  Trachea. 
22    Vagus. 

33    Left  subclavian  artery. 

40  Innominate  vein. 

41  Vertebral  artery. 

43     Costo-cervical  artery. 
45     Innominate  artery. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  90 


*%fcjfiy£i<:  •  *«F  •  »'«'''       •••»***  V'A 

^^m^j^^$l] 

^^P^;r^|^ 


?^mv-^^v?-?^ 

•'&$¥&' ^ilii 


~,   •••f.m/^<i'"i!:-- 
V  MEW<3&» 


40 


22 


MEMOIR   NO.    1,   HUNTINGTON,   1911 


DEVELOPMENT   OF   THE   THORACIC   DUCT  121 

3.     THE  AZYGOS  SEGMENT  OF  THE  THORACIC  DUCT 

This  main  part  of  the  thoracic  duct  develops  by  the  confluence 
of  extraintimal  lymphatic  anlages  which  begin  to  appear  in  the  12 
mm.  embryo,  are  clearly  marked  in  the  13  and  13.5  mm.  embryo, 
increase  in  the  14  mm.  stage,  become  confluent  to  form  larger  seg- 
ments in  the  15  and  15.5  mm.  embryos,  and  finally  unite  into  the 
plexiform  and  nearly  continuous  channels  of  the  thoracic  ducts  in 
the  16  mm.  stage.  These  extraintimal  lymphatic  anlages  develop 
at  first  along  and  around  portions  of  the  detached  and  degenerat- 
ing veins  of  the  ventro-medial  tributary  plexus  of  the  azygos  veins 
at  some  distance  from  the  latter.  Subsequently  they  extend 
dorsad  along  these  decadent  venules  and  then  come  to  lie  in  close 
apposition  to  the  ventral  aspect  of  the  main  azygos  trunks  and  the 
terminals  of  the  ventral  branches.  They  are  from  the  beginning 
genetically  distinct  and  independent  of  the  same. 

In  the  earlier  and  purely  venous  stages  the  azygos  veins  receive, 
in  addition  to  the  terminals  of  the  extensive  supracardinal  plexus, 
which  unites  the  veins  of  the  two  sides  dorsal  to  the  aorta,  larger 
dorsal  somatic  tributaries  from  the  body  walls  and  from  the  inte- 
rior of  the  vertebral  canal,  and  smaller  ventro-medial  branches 
which  drain  the  periaortic  space  close  to  the  wall  of  the  main  arte- 
rial vessel.  When  these  ventral  azygos  tributaries  appear  they 
occupy  in  general  the  position  described  as  characteristic  for 
the  cardinal  collateral  plexus  of  the  Marsupialia  (McClure.30). 

The  ventro-medial  azygos  tributary  plexus,  which  furnishes 
the  venous  line  along  and  around  which  the  first  extra-intimal 
anlages  of  the  azygos  segment  of  the  thoracic  ducts  develop,  begins 
to  appear  with  the  first  differentiation  of  the  supracardinal  plexus. 
The  recognition  of  its  course  and  extent,  and  of  the  subsequent 
changes  in  which  it  is  involved,  is  of  the  greatest  importance  to 
the  correct  interpretation  of  the  placental  thoracic  duct  develop- 
ment. The  plexus,  and  the  subsequently  more  defined  ventro- 
medial  tributary  vein,  parallel  to  the  main  azygos  trunks  in  the 
caudal  part  of  the  area  involved,  will  be  frequently  referred  to  in 
the  following  pages. 

McClure15  was  the  first  investigator  who  definitely  recognized 


122      DEVELOPMENT   OF   THE    SYSTEMIC   LYMPHATIC    VESSELS 

and  reconstructed  this  embryonal  venous  pathway.  While,  as 
previously  stated,  I  differ  from  the  conclusions  which  he  drew  in 
regard  to  the  ontogenesis  of  the  thoracic  ducts  in  the  publication 
quoted,  I  desire  to  emphasize  the  fact  that  he  for  the  first  time 
clearly  defined  the  para-azygos  venous  line,  which,  in  my  opinion, 
furnishes  the  pathway  for  the  subsequent  extra  intimal  develop- 
ment of  the  azygos  segments  of  the  thoracic  ducts. 

He  interpreted  the  thoracic  duct  in  embryos  of  the  domestic 
cat  as  a  direct  caudal  prolongation  of  the  jugular  lymph  sac,  de- 
veloped in  the  same  manner  as  the  latter,  through  fusion  of 
multiple  venous  derivatives  of  the  para-azygos  venous  line  above 
defined. 

His  recent  work  on  the  development  of  the  systemic  lymphatic 
vessels  in  the  cat,  presented  before  the  Second  International 
Anatomical  Congress  in  Brussels,  August  7th  to  llth,  1910,  and 
published  in  the  Proceedings  of  the  Congress,39  is  a  revision  of 
the  previous  publication  above  quoted,15  and  a  return,  as  regards 
the  genesis  of  the  thoracic  ducts,  to  the  original  view  which  we 
advanced  for  all  systemic  lymphatic  development  in  the  embryo 
of  the  cat  in  our  first  joint  publication  on  the  subject  in 
1906.21 

The  extraintimal  lymphatic  anlages  of  the  ducts  form  along 
and  around  the  venules  composing  the  ventromedial  tributary 
plexus  of  the  azygos  veins,  and  finally  replace  them,  while  in  the 
same  way  the  anterior  part  of  the  mesenteric  lymphatic  net  work 
has  its  origin  in  the  extraintimal  lymphatic  spaces  which  form 
around  the  caudal  continuation  of  the  ventral  plexus,  lateral  and 
ventral  to  the  aorta,  in  the  root  of  the  primitive  dorsal  meso- 
gastrium. 

It  is  necessary  to  exercise  great  care  in  the  critical  stages  in  order 
to  correctly  distinguish  between  the  degenerating  vessels  of  the 
plexus  and  the  extraintimal  lymphatic  anlages  replacing  them, 
and  to  compare  results  obtained  from  a  number  of  embryos  of 

39  C.  F.  W.  McClure:  The  Extra-intimal  Theory  and  the  Development  of 
the  Mesenteric  Lymphatics  in  the  Domestic  Cat  (Felis  domestica),  6  figs. 
Anat.  Anz.,  Erganzungsh.  z.  37.  Bd.,  Verb.  Anat.  Ges.,  24.  Vers.,  Briissel, 
1910,  S.  101-110. 


DEVELOPMENT  OF  THE  THORACIC  DUCT          123 

the  same  stage.  If  this  is  done  there  can  remain  no  doubt  that 
the  two  thoracic  ducts  in  the  embryos  of  the  cat  develop  by 
confluence  of  extraintimal  perivenous  lymphatic  spaces.  These 
anlages  appear  at  first  as  isolated  spaces,  either  surrounding  the 
retreating  veins  or  closely  applied  to  part  of  their  circumference 
and  subsequently  to  the  ventral  wall  of  the  main  azygos  trunks, 
usually  lateral  to  the  points  where  the  ventral  plexus  connected 
with  the  main  azygos  channel. 

A    General   Analysis   of   the   Development  of   the   Thoracic  Duct  in  the 

Azygos  Region 

The  clearest  preliminary  survey  of  the  development  of  the 
azygos  segment  of  the  cat's  thoracic  ducts  can  be  obtained  be 
comparing  the  series  of  reconstructions  shown  in  figs.  188  to  193, 
all  representing  the  structures  in  the  ventral  view  and  in  a  magnifi- 
cation of  225  diameters.  The  individual  sections  of  these  embryos 
will  presently  be  described  and  figured  in  detail  and  will  be  re- 
ferred to  the  reconstruction,  but  a  general  consideration  of  the 
six  figures  will,  at  this  point,  help  to  make  the  genesis  of  the  azy- 
gos segment  of  the  thoracic  ducts  clear. 

The  earliest  stage  is  a  13.5  mm.  embryo  (series  76),  shown  in 
fig.  188.  The  reconstruction  includes  the  azygos-Cuvierian  junc- 
tion of  each  side,  the  right  (3)  and  left  (6)  azygos  veins  and  their 
interazygos  supraaortic  anastomosis,  and  extends  caudad  to  the 
lower  azygos  region. 

The  intercostal  arteries  (red)  and  the  sympathetic  nerves  (1) 
are  shown.  The  numerous  extraintimal  anlages  of  the  thoracic 
ducts  (green)  incrust  the  ventral  aspect  of  the  azygos  veins  and 
of  their  anastomotic  plexus.  In  the  caudal  half  of  the  preparation 
these  lymphatic  anlages  follow  fairly  symmetrically  the  main 
azygos  trunks.  On  the  right  side  they  are  still  very  numerous  and 
separated  from  each  other,  while  the  corresponding  spaces  on  the 
left  side  have  already  become  confluent  to  form  larger,  although 
still  discontinuous,  segments  of  the  future  lymphatic  channel. 

At  the  level  marked  C  in  the  figure  the  line  of  the  lymphatic 
anlages  following  the  right  azygos  trunk  divides.  A  part  continues 


124      DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

the  original  direction,  following  the  ventral  surface  of  the  right 
azygos.  These  anlages  will  later  become  confluent  to  form  the 
intra-thoracic  portion  of  the  right  lymphatic  duct  (cf.  47  in  fig. 
193). 

Another  set  of  these  perivenous  lymphatic  spaces  diverges 
from  the  preceding  at  the  level  C  and  swings  sinistro-cephalad, 
lying  in  contact  with  the  ventral  surface  of  the  interazygos  anasto- 
motic  plexus  and  of  the  intersegmental  arteries. 

The  elements  composing  this  series  in  the  majority  of  embryos 
of  this  period,  (13.5  — 14  mm.),  have  already  become  confluent 
to  form  segments  of  considerable  length,  and  offer  very  clear  pic- 
tures of  their  extraintimal  perivenous  development,  surrounding 
radicles  of  the  ventromedial  azygos  plexus.  Thus  figs.  206  to  213 
show  transverse  sections  of  this  embryo  in  the  area  indicated  on  the 
figure  of  the  reconstruction  between  the  lines  AA  and  BB.  The 
sections  of  the  lymphatic  anlage  lying  ventral  to  the  right  inter- 
segmental artery  in  this  region  show  the  central  decadent  venule 
and  the  enveloping  extraintimal  lymphatic  space  almost  diagrama- 
tically. 

Fig.  189  is  taken  from  a  similar  reconstruction  of  a  14  mm.  cat 
embryo  (series  34  of  the  Princeton  collection) . 

The  right  (3'}  and  left  (6'}  azygos  veins  arch  ventrad  to  their 
point  of  confluence  with  the  respective  precavae  (3,  6}. 

The  interazygos  anastomosis  forms  a  dense  closely  woven  supra- 
aortic  plexus,  perforated  by  the  intersegmental  arteries.  In  gen- 
eral the  lymphatic  development  has  not  quite  reached  the  stage 
represented  by  the  preceding  series  (76),  especially  along  the 
main  right  and  left  azygos  trunks,  where  the  anlages  are  still 
relatively  few  and  of  small  extent.  On  the  other  hand,  the  lym- 
phatic line  which  in  series  76  (fig.  188)  is  seen  to  swing  mesad  to 
the  ventral  surface  of  the  interazygos  anastomosis  at  the  level  of 
C  and  thence  continues  to  ascend  sinistro-cephalad,  is  already 
well  developed  in  series  34  (fig.  189).  The  level  C  of  the  preced- 
ing figure  (188)  corresponds  in  fig.  189  to  the  upper  of  the  two 
lines  A-B.  Cephalad  of  this  level  a  well  defined  chain  of 
lymphatic  anlages  extends,  diverging  to  the  left  from  the  main 
right  azygos  line,  along  the  ventral  aspect  of  the  interazygos 


DEVELOPMENT   OF   THE   THORACIC    DUCT  125 

plexus,  between  and  in  front  of  the  series  of  right  interseg- 
mental  arteries.  As  above  stated,  the  earliest  and  best  defined 
anlages  of  the  azygos  segment  of  the  thoracic  ducts  are  usually 
found  in  this  region  in  the  14  mm.  stage.  In  this  particular 
embryo  (series  34)  the  process  of  replacement  of  the  radicles 
of  the  earlier  ventro-medial  azygos  plexus  by  the  extraintimal 
lymphatic  spaces  has  just  begun,  and  the  sections  show  the  rela- 
tion between  the  atrophying  venous  core  and  the  enveloping 
perivenous  lymphatic  anlage  clearly. 

Figs.  244  to  251  show  sections  in  the  area  marked  A-B  in  the 
reconstruction  and  afford  definite  pictures  of  this  relationship. 

Another  early  character  well  exhibited  by  this  embryo  is  the 
full  development  of  the  ventro-medial  azygos  tributary  plexus  in 
the  caudal  portion  of  the  right  side.  A  distinct  plexiform  venous 
ridge  (34)  courses  along  the  ventro-medial  border  of  the  right  azy- 
gos vein,  with  which  it  communicates  at  frequent  intervals. 
In  the  series  under  discussion  it  is  just  beginning  to  undergo  regres- 
sion and  replacement  by  perivenous  lymphatic  anlages  at  a  few 
points.  In  the  subsequent  stages  it  becomes  detached  from  the 
main  right  azygos  channel  and  forms  the  framework  upon  and 
around  which  the  large  caudal  element  of  the  thoracic  duct 
forms  on  the  right  side.  A  similar  plexiform  ridge  follows  the  left 
azygos,  but  is  usually  less  well  pronounced.  These  lines  of  para- 
azygos  venous  reticulum,  preceding  the  actual  development  of 
the  extraintimal  thoracic  ducts,  are  the  ones  which  McClure 
followed  and  described  in  the  paper  on  thoracic  duct  develop- 
ment above  quoted  (15}. 

Fig.  190,  showing  the  reconstruction  of  another  14  mm.  embryo 
(series  214),  offers  an  interesting  comparison  with  the  two  pre- 
ceding preparations.  The  embryo  is  characterized  by  advanced 
development  of  the  segment  of  the  thoracic  duct  which  diverges 
at  the  level  C  in  fig.  188  from  the  right  azygos  line  to  turn  up  and 
to  the  left  in  front  of  the  interazygos  network.  The  path  of  this 
segment  of  the  future  thoracic  duct  is  outlined  in  the  two  preced- 
ing preparations,  series  76  and  34,  by  a  line  of  detached  and  still 
isolated  lymphatic  spaces.  In  series  214  these  spaces  have,  to  a 
large  extent,  united  into  a  longer  continuous  segment  of  the  lym- 


126      DEVELOPMENT   OF   THE    SYSTEMIC   LYMPHATIC    VESSELS 

phatic  channel,  extending  cephalad  of  the  line  C  in  fig.  190  along 
the  ventral  aspect  of  the  right  intersegmental  arteries  and  of  the 
interazygos  plexus.  It  covers  the  cephalic  part  of  the  right 
ventro-medial  para-azygos  venous  ridge  (34),  the  remnants  of 
which,  detached  from  the  main  vein,  are  to  be  seen  on  section 
occupying  the  interior  of  the  perivenous  extraintimal  lymphatic 
channel  which  is  replacing  them  (Compare  figs.  214  to  240,  show- 
ing sections  from  slides  xiv  and  xv  of  series  214).  A  part  of  the 
ridge  (34)  extends  caudad  of  line  C  in  fig.  190,  but  the  process  of  its 
replacement  by  lymphatic  spaces  has  proceeded  much  further 
than  in  series  34  (fig.  189). 

Fig.  191  shows  the  ventral  view  of  the  reconstruction  of  the 
same  region  in  a  15  mm.  embryo  (series  219).  In  comparison 
with  the  13.5  and  14  mm.  stages  this  embryo  shows  more  uniform 
and  in  general  more  advanced  development  in  all  regions  of  the 
thoracic  duct  anlage.  The  individual  and  separate  lymphatic 
anlages  seen  in  series  76  and  34  (figs.  188  and  189)  have  become 
confluent  to  form  longer  and  better  defined  lymphatic  channel 
segments.  These  have  arranged  themselves  in  two  groups.  Cau- 
dad of  the  point  marked  C  in  fig.  191  they  follow  pretty  symmetri- 
cally the  ventro-medial  margin  of  the  left  and  right  azygos  trunks, 
occupying  here  the  site  of  the  earlier  ventro-medial  azygos  trib- 
utary plexus  which  they  have  in  part  secondarily  replaced.  The 
segments  are  relatively  long,  especially  on  the  left  side.  Cepha- 
lad of  the  level  marked  C  the  lymphatic  spaces  of  the  left  side 
follow  the  left  azygos  trunk,  becoming  gradually  smaller  and  more 
disconnected.  On  the  right  side  they  divide  at  C  into  two  lines. 
One  of  these  continues  upward  along  the  right  azygos  trunk  and 
arch.  The  other  and  larger  turns  c'ephalo-mesad,  and  is  prolonged 
upward  and  to  the  left,  in  front  of  the  right  intercostal  arteries 
and  the  interazygos  anastomosis.  Caudad  of  the  level  C  we  have, 
therefore,  two  lines  of  lymphatic  anlages,  folio  wing  the  right  and  left 
azygos  trunks,  while  cephalad  of  this  level  we  encounter  three,  the 
right,  left  and  intermediate.  The  former,  diverging  from  the  other 
two  in  ascending  to  right,  marks  the  path  of  the  future  right  lym- 
phatic duct.  The  two  caudal  parallel  lymphatic  lines  below  C  and 
the  central  and  left  lines  cephalad  of  this  point  become  subse- 


DEVELOPMENT   OF   THE   THORACIC   DUCT  127 

quently  connected  by  a  close  plexiform  anastomosis  and  together 
form  the  azygos  segment  of  the  thoracic  duct.  (cf.  fig.  193). 

Fig.  192  shows  the  ventral  view  of  the  central  azygos  region  in 
a  15.5  mm.  embryo,  series  143. 

The  same  plan  of  para-azygos  lymphatic  development,  with 
two  lines  caudad  and  three  cephalad  of  the  level  C,  is  presented  as 
in  the  preceding  series.  The  right  and  left  lines  are  composed  of 
relatively  long  links  of  lymphatic  channel  segments.  The  inter- 
mediate line  above  C  is,  in  the  part  shown  in  the  reconstruction, 
not  quite  as  far  advanced  as  in  the  preceding  series  219,  or  in  the 
14  mm.  embryo  (series  214,  fig.  190).  The  latter,  in  fact,  presents 
an  unusually  advanced  condition  of  this  channel,  and  illustrates 
the  fact  that  in  comparing  different  embryos  of  about  the  same 
age  lymphatic  organization  may,  in  certain  regions,  be  either 
ahead  or  behind  the  average  level  usually  attained  at  the 
period  in  question.  This  is  especially  true  in  the  earlier  lym- 
phatic stages,  in  embryos  between  13  and  15  mm.  crown-rump 
measure. 

Embryo  143  (fig.  192)  shows,  for  example,  in  comparison  with 
series  214  (fig.  190)  less  advanced  development  of  the  intermediate 
thoracic  duct  line  above  the  level  C.  Correspondingly,  the  ven- 
tro-medial  venous  ridge  (84)  of  the  right  azygos  trunk,  upon  and 
around  which  these  lymphatic  spaces  develop  and  which  the  re- 
sulting lymphatic  channel  eventually  replaces,  is  still  distinctly 
evident  in  the  former  (fig.  192),  whereas  in  the  latter  (fig.  190) 
all  but  its  caudal  portion  is  hidden  by  the  enveloping  lymphatic 
trunk. 

Fig.  192  also  shows,in  the  area  of  slide  xvii,  parts  of  the  ventral 
azygos  plexus  surrounding  the  lateral  and  ventral  circumference 
of  the  abdominal  aorta,  and  the  extraintimal  lymphatic  spaces 
forming  along  them  and  draining  into  the  right  thoracic  duct 
channel. 

Finally  the  16  mm.  embryo  (fig.  193,  series  96)  usually  marks 
the  developmental  stage  in  which  the  hitherto  isolated  and  dis- 
connected lymphatic  segments  have  united  with  each  other  into 
the  continuous  channel  of  the  azygos  portion  of  the  thoracic  and 
right  lymphatic  ducts. 


128      DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

The  latter  (47)  is  seen  in  the  cephalic  part  of  the  reconstruction 
along  the  lateral  border  of  the  right  azygos  vein.  The  formei 
shows  a  caudal  enlarged  and  fairly  symmetrical  segment,  caudad 
of  line  A  B,  in  which  the  right  and  left  thoracic  ducts,  connected 
by  several  broad  transverse  anastomoses,  follow  the  ventro-medial 
aspect  of  the  right  and  left  azygos  veins. 

The  latter  in  this  region  have  secondarily  assumed  the  supra- 
cardinal  position,  by  developing,  as  the  main  channels,  out  of 
the  preceding  interazygos  plexus.  They  hence  lie  dorsal  to  the 
lower  intersegmental  arteries.  A  remnant  of  the  former  (post- 
cardinal)  azygos  trunks,  ventral  to  the  lower  three  intercostal 
arteries,  is  seen  on  each  side  between  the  thoracic  ducts  and  the 
sympathetic  nerves  (1),  as  a  slender  longitudinal  venous  channel, 
connected  at  numerous  points  with  the  main  azygos  trunks. 
Above  the  level  of  the  line  A  B,  the  entire  and  now  united  and 
continuous  lymphatic  channel  swings  cephalo-sinistrad  and  ascends 
on  the  ventral  aspect  of  the  interazygos  anastomosis  and  of  the 
reduced  left  azygos  vein.  It  represents  the  further  development 
of  the  left  and  intermediate  lines  of  azygos  lymphatic  organization 
of  the  earlier  stages.  Each  of  these  lines  is  represented  now  by  a 
continuous  marginal  lymphatic  channel,  lateral  to  or  perforated 
by  the  intersegmental  arteries,  and  interlacing  in  a  multiple 
plexiform  anastomosis  with  its  fellow  of  the  opposite  side. 

The  mesenteric  lymphatics  of  the  dorsal  mesogastrium  (51)  are 
beginning  to  establish  their  connections  with  this  now  completed 
main  axial  lymphatic  trunk.  Further  development  of  the  same 
is  in  the  direction  of  more  definite  condensation  of  the  lymphatic 
plexus  and  relative  reduction  of  the  lumen,  as  seen  in  the  adult 
preparations  previously  figured  and  described  (cf.  figs.  95  to  99), 
p.  79. 


PART  II,  PLATES 

FIGURES  188  TO  193 


FIGURE  188 

188  Reconstruction  of  cephalic  portions  of  azygos  veins  and  anlages  of 
azygos  segment  of  thoracic  ducts  in  a  13.5  mm.  cat  embryo,  (series  76,  slide  X, 
sections  1  to  27;  slide  XI,  sections  1  to  38;  slide  XII,  sections  1  to  40;  slide  XI FT, 
sections  1  to  33;  slide  XIV,  sections  1  to  7),  X  225.  Ventral  view. 

1     Sympathetic   nerve. 

3     Right  azygos  vein,  thoracic  portion. 

6     Left  azygos  vein,  thoracic  portion. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


188 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURE  189 

189  Reconstruction  of  cephalic  portions  of  azygos  veins  and  anlages  of 
azygos  segment  of  thoracic  ducts  in  a  14  mm.  cat  embryo;  series  34  (Princeton 
Embryological  Collection),  slides  XXIV  to  XXXII,  222  sections,  X  225.  Ventral 


1  Sympathetic  nerve. 

3  Right  precava. 

3'  Right  azygos  vein,  thoracic  portion. 

6  Left  precava. 

6'  Left  azygos  vein,  thoracic  portion. 

34  Ventro-medial  azygos  plexus. 


THE  SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  101 


189 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


,  FIGURE  190 

190  Reconstruction  of  cephalic  portion  of  azygos  veins  and  anlages  of  azygos 
segment  of  thoracic  ducts  in  a  14  mm.  cat  embryo;  (series  214,  slides  XIII,  XIV, 
XV,  XVI  and  XVII),  X  225.  Ventral  view. 


1  Sympathetic  nerve. 

3  Precardinal  or  precava  of  right  side. 

3'  Right  azygos  vein,  thoracic  portion. 

6  Precardinal  or  precava  of  left  side. 

6'  Left  azygos  vein  thoracic  portion. 

34  Ventro  medial  azygos  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   102 


190 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURE  191 

191  Reconstruction  of  cephalic  portions  of  azygos  veins  and  anlages  of 
azygos  segment  of  thoracic  ducts  in  a  15  mm.  cat  embryo;  (series  219,  slides 
XIV,  XV,  XVI  and  XVII),  X  225.  Ventral  view. 

1    Sympathetic  nerve. 


PLATE   103 


191 


MEMOIR  NO.   1,  HUNTINGTON,  1911 


FIGURE  192 

192  Reconstruction  />f  cephalic  portions  of  azygos  veins  and  anlages  of 
azygos  segment  of  thoracic  ducts  in  a  15.5  mm.  cat  embryo;  (series  143,  slides 
XIV,  XV,  XVI,  XVII  and  XVIII)  X  225.  Ventral  view. 

34    Ventro-medial  azygos  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  104 


XVIIT. 


192 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURE   193 

193     Reconstruction  of  azygos  veins  and  of  thoracic  and  right  lymphatic  ducts 
In  a  16  mm  cat  embryo;  (series 96,  slides  VII  to  XVI)  X  225.     Ventral  view. 

1  Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

47  Right  lymphatic  duct. 

51  Mesenteric  lymphatics. 


THE   SYSTEMIC'   LYMPHATIC   VKSSKI.S 


PLATE   105 


193 


MEMOIR   NO.    1,   HUNTINGTON,   1911 


DEVELOPMENT  OF  THE  THORACIC  DUCT  129 

B.      Detailed  consideration  of  the  individual  stages  in  the  develop- 
ment of  the  azygos  segment  of  the  thoracic  duct 

Figs.  194  and  195  show  transverse  sections  of  the  middle  thoracic 
region  in  an  11  mm.  cat  embryo  (series  213,  slide  xi,  sections 
9  and  10,  X  225.)  The  right  and  left  azygos  veins  (3,  6)  lie  ventral 
to  the  sympathetic  nerves  (1)  on  each  side  of  the  aorta  (7). 
Between  the  latter  and  the  right  azygos  vein  are  seen  portions  of 
the  ventro-medial  azygos  plexus  (34). 

Figs.  196  and  197  show  transverse  sections  of  the  same  region  of 
this  embryo  further  caudad  at  the  level  of  a  pair  of  dorsal  inter- 
segmental  arteries  (2)  (series  213,  slide  xi,  sections  27  and  29,  X 
225).  The  main  azygos  veins  (3,  6}  are  reduced  in  comparison 
with  the  previous  sections,  while,  on  the  other  hand,  the  radicles  of 
the  ventro-medial  azygos  plexus  (34)  are  increased  in  number 
and  size.  This  is  especially  so  on  the  right  side,  in  the  space 
between  sympathetic  nerve  (1)  and  intersegmental  artery  (2) 
dorsad,  aorta  (7)  mesad,  and  main  azygos  trunk  (3)  laterad.  In 
the  later  stages  (14  mm.)  this  is  the  site  of  the  earliest  and  most 
distinct  extraintimal  replacement  of  the  venous  plexus  by  the 
lymphatic  anlages  of  the  right  thoracic  duct  (cf.  figs.  214  to  251). 

The  full  development  of  the  ventro-medial  azygos  plexus  is  seen 
in  the  12  mm.  stage.  Figs.  198,  199  and  200  show  three  succes- 
sive transverse  sections  of  a  12  mm.  embryo  (series  217,  slide  x, 
section  27,  28  and  29,  X  225)  at  the  [level  of  origin  of  a  pair  of 
dorsal  intersegmental  arteries  (2).  Ventrad  of  these  and  of  the 
sympathetic  strand  (1),  in  the  interval  between  the  main  azygos 
trunks  (3,  6}  and  the  aorta  (7)  are  numerous  radicles  of  the  plexus 
(34)  -  The  same  has  developed  into  a  more  extensive  reticulum, 
compared  with  the  preceding  stage,  and  now  occupies  the  typical 
ventro-medial  position  in  relation  to  the  parent  azygos  trunks. 
Figs.  201,  202  and  203  show  three  sections  of  the  same  embryo 
further  cephalad  (series  217,  slide  x,  sections  18,  30  and  31). 
They  are  of  interest  because  they  illustrate  the  condition  of  part 
of  the  plexus  just  prior  to  its  replacement  by  the  extraintimal 
anlages  of  the  thoracic  ducts.  Some  of  the  components  of  the 
plexus,  occupying  the  site  of  the  future  lymphatic  channel,  begin 


130      DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

to  lose  their  connection  with  the  azygos  trunks,  and  appear  as 
partially  detached  venous  elements  closely  applied  to  the  ventro- 
medial  wall  of  the  main  vein. 

Thus  the  ventro-medial  tributary  34  in  fig.  202,  (slide  x,  sec- 
tion 30),  still  in  open  communication  with  the  main  right  azygos 
vein  (3),  is  seeninthe  next  section  (fig.  201,  slide  x,  section  31)  to  be 
separated  from  the  same,  and  can  be  followed  for  a  considerable 
distance  caudad,  closely  applied  to  the  ventro-medial  aspect  of 
the  parent  trunk,  but  no  longer  opening  into  the  same  or  con- 
nected with  adjacent  elements  of  the  azygos  plexus.  A  venule  of 
this  type  will,  in  the  succeeding  stages,  form  the  line  along  and 
around  which  the  extraintimal  anlages  of  the  thoracic  duct  will 
develop. 

Two  successive  transverse  sections  of  the  central  thoracic 
region  in  a  13.5  mm.  embryo  (series  189,  ^lide  x,  sections  15  and 
16,  X  225)  are  shown  in  figs.  198  and  199.  The  ventro-medial 
azygos  venous  plexus  (#4)  is  still  prominent,  especially  on  the  right 
side,  between  right  azygos  vein  (3)  and  aorta  (7).  Some  of  its 
ventral  and  lateral  components  (4)  are,  however,  detached  from 
the  main  plexus  and  are  beginning  to  be  surrounded  by  the  early 
extraintimal  anlages  of  the  thoracic  duct  (<5). 

In  another  embryo  of  this  period  (series  76),  extraintimal  lym- 
phatic development  in  the  axygos  region  is  further  advanced  than 
is  usually  the  case  in  the  13.5  mm.  stage,  i  igs.  206  to  213  inclu- 
sive show  transverse  sections  through  the  middle  thoracic  region 
of  this  embryo  (series  76,  slide  xi,  sections  15,  16,  17,  19,  21,  22, 
23,  28,  X  300).  The  microphotographs  are  to  be  referred  to  the 
ventral  view  of  the  reconstruction  of  slides  x,  x',  xi ,  xiii, 
and  part  of  side  xiv,  (155  15  n  sections)  shown  in  fig.  188  and 
are  included  within  the  area  bounded  in  this  figure  by  the  lines 
A-B.  They  show  especially  the  development  of  the  prominent 
extraintimal  intermediate  segment  of  the  thoracic  duct  an!age 
on  the  ventral  aspect  of  the  interazygos  plexus  and  of  the  fourth 
intercostal  artery  of  the  right  side.  Fig.  206  (section  15  of  slide 
xi)  shows  the  right  azygos  vein  (3),  the  aorta  (7)  and  the  well 
developed  interazygos  plexus  (15).  A  radicle  of  the  latter  (4), 
in  the  interval  between  the  structures  named,  is  almost  completely 


DEVELOPMENT  OF  THE  THORACIC  DUCT  131 

surrounded  by  the  extraintimal  anlage  (5)  of  the  intermediate 
segment  of  the  azygos  portion  of  the  thoracic  duct.  The  extrain- 
timal anlage  of  the  right  segment  of  the  duct  (not  labelled  in 
figure)  is  seen  in  this  and  some  of  the  succeeding  sections  ventral  to 
the  right  azygos  vein,  surrounding  an  atrophying  radicle  of  the 
ventro-medial  azygos  plexus.  The  two  succeeding  sections  (16 
and  17  of  slide  xi,  figs.  207  and  208)  show  the  same  extraintimal 
lymphatic  anlage  and  the  enclosed  venous  radicle  in  its  relation  to 
the  right  intercostal  artery  (2  in  fig.  208),  and  it  can  be  followed 
through  the  remaining  figures  (209  to  213)  always  in  the  same 
position,  in  the  interval  between  the  interazygos  plexus,  the  aorta, 
and  the  right  azygos,  and  ventral  to  the  right  intercostal  arteries. 
In  stages  slightly  less  developed  than  the  present  embryo  the  lym- 
phatic anlages  of  the  central  thoracic  duct  division  are  usually 
interrupted  at  the  level  of  the  intersegmental  arteries,  and  present 
in  many  cases  a  regular  segmental  character.  Later,  as  in  the 
present  instance,  these  segmental  anlages  become  confluent 
across  the  ventral  aspect  of  the  intercostal  arteries.  The  figure  of 
the  reconstruction  (fig.  188)  still  shows  the  earlier  segmental 
arrangement  of  the  duct  anlages  in  the  cephalic  part,  in  relation 
to  the  first  three  right  intercostal  arteries. 

In  the  succeeding  stage,  14  mm.,  the  isolated  and  interrupted 
lymphatic  anlages  of  the  13.5  mm.  stage  have  usually  coalesced 
to  form  much  longer  continuous  channel  segments. 

It  is  necessary  to  examine  a  large  number  of  successive  sections 
in  many  embryos  in  order  to  become  convinced  of  this  marked 
advance  in  lymphatic  development.  Thus,  for  example,  the  lym- 
phatic anlage  of  the  azygos  segment  of  the  thoracic  duct  just 
described  in  certain  sections  of  the  preceding  13.5  mm.  embryo 
(series  76,  figs.  206  to  213),  is  found  in  the  identical  position  and 
relation  to  surrounding  structures,  and  much  more  fully  developed 
in  the  14  mm.  embryo  shown  in  figs.  214  to  240  inclusive,  and  in 
reconstruction  in  fig.  190. 

As  a  matter  of  fact  every  phase  in  the  early  extraintimal  devel- 
opment of  the  thoracic  duct  anlage  can  be  perfectly  illustrated  by 
selections  from  the  72  sections  composing  slides  xiv  and  xv  of 
this  series. 


132      DEVELOPMENT    OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

Figs.  214  to  219  inclusive  show  transverse  sections  in  the  central 
thoracic  region  in  this  embryo,  (series  214,  slide  xiv,  sections 
15,  16,  17,  19,  20,  22,  X  225),  in  which  the  extraintimal  thoracic 
duct  development  and  its  relation  to  the  atrophying  central  venule 
of  the  ventro-medial  azygos  plexus  is  shown  at  the  height  of  its 
development.  In  the  interval  between  aorta,  right  azygos  vein 
and  oesophagus  all  six  sections  show  the  empty  and  partially 
collapsed  central  endothelial  tube  of  the  decadent  ventro-medial 
azygos  venule  (4),  surrounded  by  the  extraintimal  lymphatic 
anlage  of  the  thoracic  duct  (5),  about  to  replace  it  topographically. 
The  central  atrophying  venule  (4)  is  here  still  of  large  size, 
although  empty  and  completely  separated  from  the  functional 
azygos  venous  channels.  It,  together  with  the  enveloping  peri- 
venous  extraintimal  lymphatic  anlage  of  the  thoracic  duct  («5), 
forms  a  conspicuous  histological  object  in  the  field  above  defined, 
between  aorta,  oesophagus,  right  azygos  vein  and  interazygos 
plexus.  Figs.  220  to  224  inclusive  show  transverse  sections  of  the 
same  embryo  further  caudad  on  the  same  slide  (series  214,  slide 
XIV,  sections  26,  27,  28,  32  and  34,  x  225).  The  central  atro- 
phying venule  (4)  in  the  interior  of  the  replacing  extraintimal  peri- 
venous  lymphatic  space  (5}  is  undergoing  further  reduction  and 
diminution  in  size  and  extent,  until,  in  fig.  224,  it  has  receded  to 
an  insignificant  tab  of  tissue  (4)  still  attached  at  one  point  to  the 
interior  of  the  endothelial  lining  of  the  lymphatic  space  (5).  The 
reduced  central  venous  remnant  (4)  and  the  surrounding  extrain- 
timal lymphatic  anlage  (5}  have  shifted  in  these  five  sections  dorsad 
until  they  come  into  apposition  with  the  ventral  aspect  of  the 
broad  interazygos  anastomosis  in  the  interval  between  the  same, 
the  aorta  and  the  oesophagus. 

In  figs.  225  to  229  inclusive  five  successive  sections  from  the 
beginning  of  the  same  slide  are  given  (series  214,  slide  xiv,  sec- 
tions 1,  2,  3,  4,  and  5,  X  225).  This  series  corresponds  to  the  one 
just  discussed,  from  the  caudal  part  of  the  same  slide.  The  cen- 
tral decadent  venule  (4)  in  sections  1  and  2  (figs.  225  and  226) 
can  still  be  made  out  in  the  interior  of  the  peri  venous  extraintimal 
lymphatic  space  (5),  but  in  the  succeeding  sections  3  and  4  (figs. 
227  and  228)  the  latter  alone  occupies  the  field,  showing  the  elimi- 


DEVELOPMENT  OP  THE  THORACIC  DUCT          133 

nation  of  the  antecedent  venous  kernel,  and  the  establishment  of 
a  lymphatic  channel  with  clear  and  empty  lumen.  In  the  follow- 
ing section,  5,  (fig.  229)  the  lymphatic  channel  ends  blindly  in  the 
mesoderm,  indicating  one  of  the  intervals  dividing  the  still  separ- 
ate and  distinct  links  in  the  chain  of  lymphatic  segments  which  are 
forming  in  this  stage  along  the  line  of  the  future  continuous 
thoracic  ducts.  (Of.  reconstruction  of  this  embryo,  shown  in  fig. 
190,  at  level  of  first  right  intercostal  artery). 

Figs.  230  to  235  inclusive  show  transverse  sections  from  the 
central  region  of  the  next  slide  of  the  same  embryo  (series  214, 
slide  xv,  sections  10,  11,  14,  16,  19,  21,  X  225).  Sections  10  and 
11  (figs.  230  and  231)  repeat  practically  the  conditions  above 
observed  and  recorded  in  sections  15,  16,  17,  19,  20  and  22  of 
slide  xiv.  A  large  empty  central  endothelial  bag  (4)  represents 
the  decadent  ventro-medial  azygos  tributary  around  which  the 
extraintimal  lymphatic  anlage  of  the  thoracic  duct  (5)  is  forming. 
In  sections  14,  16  and  19  (figs.  232,  233  and  234)  both  the  central 
venous  kernel  (4)  and  the  replacing  perivenous  lymphatic  space 
(5)  are  diminishing,  just  as  they  are  doing  in  figs.  220  to  224, 
sections  26,  27,  28,  32  and  34  of  the  preceding  slide  xiv  of  this 
embryo.  In  section  21  of  slide  xv  (fig.  235)  the  perivenous 
lymphatic  space  stops,  and  only  the  central  venous  kernel  (4}, 
still  connected  with  the  ventro-medial  azygos  plexus  of  the  right 
side,  persists. 

Finally  figs.  236  to  240  inclusive  give  five  successive  sections  of 
the  same  embryo  in  the  terminal  part  of  slide  xv  (series  214, 
slide  xv,  sections  27,  28,  29,  30  and  31,  X  225),  in  which  the  stage 
of  the  early  formation  of  the  extraintimal  anlage  of  the  azygos 
portions  of  the  thoracic  duct  is  shown.  The  decadent  ventro- 
medial  azygos  tributary  (4)  is  almost  completely  separated  from 
the  azygos  plexus,  although  the  path  of  its  original  connection 
with  the  same  can  still  be  traced  by  the  arrangement  of  the  peri- 
venous mesodermal  cells.  The  extraintimal  lymphatic  anlage 
of  the  thoracic  duct  (5)  develops  at  first  on  the  lateral  aspect  of  the 
atrophying  component  of  the  ventro-medial  azygos  plexus,  and  at 
some  distance  ventral  to  the  main  azygos  trunks  and  to  the  inter- 
azygos  anastomosis.  This  series  is,  therefore,  of  considerable 


134      DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

interest,  as  exhibiting,  at  different  levels  in  the  same  embryo,  the 
following  phases  of  early  extraintimal  replacement  of  ventro- 
medial  azygos  tributaries  by  the  thoracic  duct  anlages : 

1.  Detachment  of  venous  elements  of  the  plexus,  as  empty 
endothelial  tubes,  surrounded  by  extraintimal  lymphatic  anlages : 
Slide  xiv,  sections  15,  16, 17, 19,  20,  22,  (figs.  214  to  219  inclusive). 
Slide  xv,  sections  10  and  11,  (figs.  230  and  231). 

2.  Gradual  recession    of    degenerating    central    venule,    and 
approach  of  same   and  of  surrounding  extraintimal  lymphatic 
space  to  ventral  aspect  of  main  azygos  system:     Slide  xiv,  sec- 
tions, 26,  27,  28,  32,  and  34,  (figs.  220  to  224  inclusive).     Slide 
xv,  sections  14,  16,  and  19  (figs.  232,  233  and  234) 

3.  Elimination    of    central    atrophying    venous    kernel   with 
persistence  of  clear  lumen  of  lymphatic  channel  segment:  Slide 
xiv,  sections  1,  2,  3,  and  4,  (figs.  225,  226,  227  and  228). 

4.  Blind  ending  of  lymphatic   channel  anlage  and  develop- 
ment of  interval  between  the  still  disjointed  links  of  the  future 
continuous  lymphatic  chain  of  the  thoracic  duct:  Slide  xiv,  sec- 
tion 5,  (fig.  229)  and  reconstruction  (fig.  190). 

5.  Blind  ending  of  extraintimal  perivenous  lymphatic  anlage 
with  persistence  of  ventro-medial  azygos  tributary  venule   (4) : 
Slide  xv,  section  21  (fig.  235). 

6.  Early  stage  of  development  of  azygos  segment  of  thoracic 
duct,  in  which  the  same  appears  as  an  extraintimal  lymphatic 
space  (5}  closely  applied  to  the  lateral  circumference  of  a  compo- 
nent of  the  ventro-medial  azygos  venous  plexus  (4),  still  in  com- 
munication with  the  axial  venous  trunks,  but  destined  subse- 
quently to  be  separated  from  them  and  to  undergo  entire  extrain- 
timal replacement  by  the  surrounding  lymphatic  space:  Slide  xv, 
sections  27,  28,  29,  30  and  31   (figs.  236  to  240  inclusive). 

Another  feature  of  the  early  development  of  the  azygos  segment 
of  the  thoracic  ducts,  strikingly  illustrated  by  the  embryo  under 
discussion,  is  the  segmental  type  of  the  originally  isolated  and 
independent  perivenous  extraintimal  lymphatic  development. 
Thus  in  the  selected  sections  of  the  two  slides  xiv  and  xv  just 
described  the  following  succession  of  conditions  is  to  be  noted. 
Sections  1  and  2  (figs.  225  and  226)  lead  up,  at  the  caudal  end 


DEVELOPMENT    OF   THE    THORACIC    DUCT  135 

of  a  link  of  the  chain,  by  gradual  reduction  of  the  central  atro- 
phying vein,  to  a  point  (sections  3  and  4,  figs.  227  and  228,)  where 
the  same  stops,  and  only  the  perivenous  lymphatic  anlage  (5}  con- 
tinues. The  latter  also  ceases  blindly  in  the  following  section, 
(5,  fig.  229),  and  then  follows  an  interval  in  which  no  lymphatic 
anlages  exist. 

These  gradually  appear  again,  in  the  same  situation,  and  reach 
their  full  development  about  the  middle  of  this  slide  in  sections 
15,  16,  17,  19,  20  and  22  (figs.  214  to  219  inclusive). 

In  the  caudal  part  of  the  same  slide  both  the  central  decadent 
vein  core  (4)  and  the  enveloping  lymphatic  space  (5)  again  dimin- 
ish, and,  at  the  same  time,  approach  the  ventral  aspect  of  the  inter- 
azygos  plexus,  in  sections  26,  27,  28,  32,  and  34  (figs.  220  to  224 
inclusive).  They  continue  in  this  condition  in  the  beginning  of 
slide  xv.  Further  caudad  the  lymphatic  anlage  again  increases 
in  size  and  rapidly  reaches  its  former  degree  of  development. 
Thus  section  10  of  slide  xv  (fig.  230)  corresponds  to  section  15  of 
slide  xiv  (fig.  214)  in  the  extent  and  relations  of  both  the  central  atro- 
phying venous  core  (4)  and  the  enveloping  extraintimal  lymphatic 
space  (5),  and  the  same  condition  is  maintained  in  the  succeed- 
ing sections  11,  14,  16  and  17  of  slide  xv,  (figs.  231,  232,  233  and 
234)  which  compare  strictly  with  sections  16,  17,  19,  20  and  22  of 
slide  xiv,  (figs.  215,  216,  217,  218  and  219). 

Sections  10  and  11  of  slide  xv  (figs.  230  and  231)  show  especially 
well  the  relation  of  the  atrophying  central  venule  (4}  and  the  sur- 
rounding extraintimal  lymphatic  space  (5)  to  the  right  azygos 
trunk  (3),  the  aorta  (7)  and  the  right  intersegmental  artery  (2). 
Comparison,  for  example,  with  corresponding  sections  of  the  pre- 
ceding series  76  will  demonstrate  the  identity  of  both  anlages  in  the 
two  embryos  (cf.  series  76,  slide  xi,  sections  16, 17  and  19,  (figs. 
207,  208  and  209). 

The  relations  of  the  early  thoracic  duct  anlages  are  clearly  evi- 
dent in  the  ventral  view  of  the  reconstruction  of  embryo  214, 
shown  in  fig.  190. 

The  lymphatic  anlage  of  the  left  side,  forming  the  beginning 
of  the  caudal  part  of  the  left  thoracic  duct,  smaller  and  less 
developed  in  this  stage,  compared  with  the  corresponding  struc- 


136        DEVELOPMENT  OF  THE  SYSTEMIC  LYMPHATIC  VESSELS 

ture  on  the  right,  begins  to  make  its  appearance  in  slide  xv  of 
this'  embryo  (series  214,  section  33)  in  relation  to  a  rudimentary 
ventral  tributary  of  the  left  azygos  vein  (section  32) .  It  can  be 
followed  through  the  rest  of  the  slide  to  section  36,  and  in  the 
succeeding  slide  xvi  to  section  7.  It  reappears  in  section  15  of 
slide  xvi,  again  in  association  with  a  reduced  ventral  azygos 
branch,  and  continues  to  section  26,  where  it  seems  to  end.  It 
reappears  in  the  following  section  (27)  again  as  the  extraintimal 
envelope  of  a  small  retrograding  ventral  azygos  branch,  and  in- 
creases rapidly  in  size,  ending  in  section  30.  It  again  appears  in 
section  33,  and  can  be  traced  with  frequent  interruptions  from  this 
point  caudad,  diminishing  in  size  and  continuity,  while  conversely 
the  ventral  azygos  tributaries  of  this  area  are  larger  and  better 
developed  (cf.  left. side  of  reconstruction,  fig.  190). 

Certain  14  mm.  embryos,  in  which  the  development  of  the  thor- 
acic duct  anlages  in  the  middle  and  lower  thoracic  region  has  not 
yet  reached  the  condition  usually  encountered  in  average  embryos 
of  this  period,  furnish  excellent  examples  of  the  early  appearance 
of  the  first  lymphatic  spaces  in  their  relation  to  the  components 
of  the  ventro  medial  azygos  tributary  plexus,  which  they  are  des- 
tined to  eventually  replace. 

Thus,  in  another  14  mm.  embryo  (series  127,  slide  x,  sections 
3,  4,  and  10,  X  225),  shown  in  transverse  section  in  figs.  241, 
242,  and  243,  the  ventro-medial  azygos  plexus  (34  in  fig.  241)  is 
still  well  preserved  and  in  open  communication  with  the  main  right 
azygos  trunk.  The  following  section  (fig.  242)  shows  the  same 
conditions,  but  a  small  extraintimal  lymphatic  space  (5)  appears 
in  relation  to  one  of  the  component  venules  (4)  of  the  peleus, 
applied  to  its  dorso-lateral  circumference.  The  same  beginning 
of  extraintimal  lymphatic  space  development  in  relation  to  azygos 
tributaries  is  seen  further  caudad  in  the  same  slide  of  this  embryo 
(figs.  243,  series  127,  slide  x,  section  10). 

One  of  the  best  examples  of  the  early  stages  of  development  of 
the  thoracic  duct  anlages  in  relation  to  the  ventro-medial  tribu- 
taries of  the  azygos  veins  is  afforded  by  a  14  mm.  embryo  (series 
34  of  the  Princeton  University  embryological  collection).  I  owe 
the  opportunity  of  examining  and  reconstructing  this  remarkably 


DEVELOPMENT    OF    THE    THORACIC    DUCT  137 

fine  series  to  the  kindness  of  my  colleague,  Prof.  C.  F.  W.  McClure. 
The  embryo  shows  in  the  mediastinal  and  in  the  cephalic  portion 
of  the  azygos  region  the  typical  extraintimal  formation  of  the 
thoracic  duct  anlages,  while  in  the  more  caudal  part  the  ventro- 
medial  tributary  venous  plexus  of  the  azygos  trunks  is  still  fully 
developed  and  not  yet  invaded  by  the  enveloping  and  replacing 
lymphatics  anlages.  Intermediate  between  these  two  districts 
are  areas  where  the  decadent  ventro-medial  azygos  venous  tribu- 
taries can  be  clearly  traced  into  the  surrounding  replacing  extrain- 
timal lymphatic  plexus.  The  general  disposition  of  the  azygos 
veins  and  of  the  thoracic  duct  anlages  in  this  embryo  is  shown  in  the 
ventral  view  of  the  reconstruction  of  slides  (xxiv  to  xxxii  given  in 
fig.  189. 

The  perivenous  lymphatic  spaces  are  fully  established  in  the 
cephalic  part  of  the  azygos  and  in  the  preazygos  portions,  al- 
though not  yet  joined  into  longer  channel  segments.  In  the  caudal 
area  the  plexus  of  the  ventro-medial  azygos  tributaries  predomi- 
nates, while  the  accompanying  and  enveloping  extraintimal  lym- 
phatic anlages  are  much  reduced  in  size  and  number.  Intermed- 
iate between  these  two  areas,  and  corresponding  to  slides  xxvii 
and  xxxviii,  lymphatic  development  is  actively  proceeding,  especi- 
ally along  the  right  azygos  tributary  venous  line  34  in  figure  189, 
by  the  formation  of  extraintimal  mesenchymal  spaces  around  the 
venules  of  the  azygos  plexus.  Sections  in  this  area  furnish  con- 
clusive early  pictures  of  the  decadent  venous  radicles,  almost  com- 
pletely detached  from  the  main  channel  and  surrounded  by  peri- 
venous  lymphatic  anlages.  Figs.  246  to  251  show  six  successive 
transverse  sections  (17  to  22  inclusive)  of  slide  xxviii,  in  the 
region  indicated  in  the  figure  of  the  reconstruction  (fig.  189)  by 
the  lines  A-B. 

In  fig.  246  (section  17,  X  225)  the  small  central  venous  rem- 
nant (4)  surrounded  by  the  extraintimal  lymphatic  anlage  (5) 
lies  in  the  interval  between  aorta  (7)  mesad,  right  azygos  vein  (3) 
laterad,  oesophagus  (8)  ventrad,  and  elements  of  the  interazygos 
anastomosis  dorsad. 

In  section  18  (fig.  247)  the  same  structures  are  seen.  The  cen- 
tral vein  (4)  in  the  interior  of  the  enveloping  lymphatic  anlage 


138      DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC   VESSELS 

(r5)  is  larger  and  still  contains  a  number  of  red  blood  cells.  In  the 
four  succeeding  sections,  19,  20,  21  and  22  (figs.  248,  249,  250  and 
251)  the  former  line  of  communication  of  the  decadent  venule  (4) 
with  the  functional  azygos  channel  can  still  be  distinctly  traced  as 
a  strand  of  connective  tissue  cells  joining  it  to  the  beginning  of  the 
right  interazygos  plexus.  The  separation  of  the  venous  radicle 
undergoing  extraintimal  lymphatic  replacement  has  just  been 
accomplished  in  this  area. 

The  six  sections  of  this  embryo  shown  in  figs.  246  to  251  should 
be  compared  with  the  slightly  more  advanced  14  mm. embryo  214; 
where,  e.g.,  in  figs.  230,  231,  232,  214,  215,  216,  217,  218  and  219 
exactly  equivalent  sections  are  given,  showing  the  next  step  in  ex- 
traintimal lymphatic  development  in  this  region.  The  atrophying 
venule  (4)  in  the  earlier  embryo  (series  34)  still  contains  red 
blood  cells  and  still  betrays  its  original  connection  with  the  func- 
tional venous  channels.  In  the  genetically  slightly  older  embryo 
(series  214)  the  same  structure  appears  now  as  an  empty  endothe- 
lial  bag  (4),  completely  detached  from  the  azygos  veins.  In  both 
embryos  this  decadent  venous  radicle  is  surrounded  by  the  de- 
veloping extraintimal  lymphatic  space  (5}.  The  comparison  of 
the  sections  shows  every  step  in  the  process  of  development  in 
these  two  closely  connected  stages.  The  reduced  photographic 
reproductions  do  not  give  the  clear  and  unmistakable  pictures 
presented  by  the  actual  sections,  owing  to  the  loss  of  the  differ- 
ential stain  and  of  the  focal  adjustment.  Still  the  contour  of  the 
venous  core,  undergoing  atrophy  and  replacement  by  the  extrain- 
timal lymphatic  anlage,  its  content  of  red  blood  cells  and  its 
recently  interrupted  connection  with  the  main  azygos  vein  in  the 
younger  embryo  (series 34),  can  be  followed  with  a  sufficient  degree 
of  clearness  and  can  be  contrasted  with  the  conditions  presented 
by  the  succeeding  stage  (series  214). 

Figs.  244  and  245  give  two  successive  sections  from  the  caudal 
part  of  the  thoracic  region  in  series  34  (slide  xxxi,  sections  18 
and  19,  X  225)  in  which  the  earlier  conditions,  preceding  the  first 
appearance  of  the  lymphatic  anlages  of  the  thoracic  duct  in  the 
azygos  segment,  are  shown. 

Between  the  right  azygos  vein  (3}  and  the  aorta  (7)  are  seen 


DEVELOPMENT  OF  THE  THORACIC  DUCT          139 

the  components  of  the  ventro-medial  azygos  plexus  (4),  partially 
separated  from  the  main  venous  trunks,  but  not,  as  yet,  sur- 
rounded by  extraintimal  lymphatic  anlages,  as,  further  cephalad, 
(slide  xxviii)  in  the  sections  just  described,  (figs.  246  to  251). 

The  15  mm.  and  15.5  mm.  embryos  show,  in  the  majority  of 
instances,  an  advance  over  the  preceding  stage  in  two  directions : 

I.  The  central  venous  core  of  the  14  mm.  embryo  is  further 
reduced  or  entirely  eliminated,  leaving  the  lymphatic  anlage, 
which  formerly  surrounded  it,  with  a  clear  lumen. 

II.  The  individual  scattered  lymphatic  areas  have  united  to 
form  longer  segments  of  the  future  lymphatic  channel  system. 
This  condition  is  well  shown  in  the  ventral  view  of  the  reconstruc- 
tion of  an  average  15  mm.  embryo  (series  219)  in  fig.  191  (cf. 
supra,  p.  126). 

Figs.  252  to  258  inclusive  show  transverse  sections  of  the  lower 
thoracic  region  in  a  15.5  mm.  cat  embryo,  (series  143,  slide  xviii 
section  7,  11,  12,  13,  14;  slide  xvii,  sections  31  and  32,  X  225), 
and  fig.  192  gives  the  ventral  view  of  the  reconstruction  of  the 
azygos  region  in  this  embryo,  comprising  slides  xiv,  xv,  xvi, 
xvii,  and  xviii. 

The  sections  (figs.  252  to  258)  show  the  following  changes  in  the 
vascular  structures,  compared  with  the  preceding  stages 

I.  The  right  (3)  and  left  (6)  azygos  veins  are  concentrated, 
more  sharply  defined  and  relatively  smaller,  although  still  equally 
developed  on  both  sides. 

II.  The  interazygos  anastomosis  is  still  well  developed  and 
uniform  (cf.  also  fig.  192). 

III.  The  entire  azygos  complex  is  much  more  closely  applied 
to  the  dorsal  and  dorso-lateral  circumference  of  the  aorta  (7), 
resulting  in  the  practical  obliteration  of  the  interval  between  the 
main  veins  and  the  artery  seen  in  the  preceding  stages. 

IV.  This  topographical  rearrangement  has  forced  the  ventro- 
medial  azygos  tributaries,  where  they  still  persist  (34  in  figs.  252, 
253,  257),  and  the  thoracic  duct  anlage  (36)  to  pass  from  the 
ventro-medial  to  the  ventral  aspect  of  the  main  azygos  trunks. 

V.  Both  azygos  veins  lie  in  the  region  ventro-lateral  to  the  inter- 
segmental  arteries.    The  supra-aortic  area -between  them  is  still 


140       DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

occupied  by  the  interazygos  (supra-cardinal)  anastomosis  (cf. 
infra,  figs.  261  and  262). 

VI.  The  sections  taken  from  the  caudal  portion  of  the  thoracic 
region  (slides  xvii  and  xviii)  show  the  right  and  left  thoracic 
duct  anlages  (86)  following  the  ventral  aspect  of  the  respective 
azygos  veins  (cf.  fig.  192).  They  are  not  yet  united  into  a  continu- 
ous channel,  but  their  lumen  is  clear,  without  trace  of  the  venous 
kernel  around  which  they  developed. 

Fig.  252  (slide  xviii,  section  7)  shows  remnants  of  the  ventro- 
medial  azygos  plexus  (34)  emptying  on  both  sides  into  the  azy- 
gos trunks.  Lateral  to  these  venous  radicles  lies  the  thoracic 
duct  anlage  of  each  side  (36). 

In  section  11  of  the  same  slide  (fig.  253)  the  right  thoracic 
duct  anlage  has  enlarged  and  presents  a  beautifully  clear  picture 
of  the  relation  of  this  structure  to  the  rightazygosvein  at  this  stage. 

On  the  left  side  the  conditions  are  as  in  the  preceding  figure, 
both  persistent  ventral  venous  tributary  (84)  and  left  thoracic  duct 
anlage  (36)  lying  side  by  side. 

In  the  two  succeeding  sections,  12  and  13,  (figs.  254  and  255)  the 
right  thoracic  duct  continues  well  developed  and  presents  a 
pointed  dorso-mesal  prolongation  indicative  of  its  situation  in  the 
earlier  stages,  on  the  mesal  aspect  of  the  vein,  between  it  and  the 
aorta,  and  ventral  to  the  interazygos  anastomosis,  (cf.  series 
34  and  214).  The  left  duct  anlage  continues  as  a  small  channel. 

In  section  18,  (fig.  256)  both  right  and  left  lymphatic  anlages 
cease  as  distinct  channels,  marking  one  of  the  intervals  between 
the  still  disconnected  segments  of  the  future  continuous  duct. 

Figs.  257  and  258  (sections  31  and  32  of  slide  xvii)  show  on 
alternating  sides  small  thoracic  duct  anlages  (86),  and  in  the  root 
of  the  dorsal  mesogastrium  sections  of  the  well-developed  anterior 
mesenteric  lymphatics  (51).  Some  of  the  later  stages  (series  253, 
figs.  265  to  270)  will  show  the  full  development  of  these  mesen- 
teric channels  and  their  confluence  with  the  thoracic  duct. 
This  area,  is,  however,  responsible  for  the  development  of  what 
I  have  above  defined  as  the  post-azygos  segment  of  the  thoracic 
duct  and  will  hence  be  considered  in  detail  in  the  second  volume 
of  this  series. 


DEVELOPMENT    OF    THE    THORACIC    DUCT  141 

In  comparison  with  the  series  just  considered  figs.  259  and 
260  show  transverse  sections  of  the  lower  thoracic  region  of  series 
258,  slide  xviii,  sections  1  and  9,  X  225.  This  embryo  is  rated 
as  17  mm.  in  crown-rump  length,  but  the  lymphatic  develop- 
ment of  the  azygos  region  is  relatively  retarded  and  only  slightly 
in  advance  of  the  conditions  presented  by  the  15.5  mm,  series 
143.  Direct  comparison  of  figs.  252  to  258  with  figs.  259  and 
260  will  show  this  correspondence,  both  at  the  lev^l  of  the  inter- 
segmental  arteries  (2  in  fig.  260),  and  in  the  intervals  between  them 
(fig.  259).  In  the  older  embryo  the  right  and  left  thoracic  duct  an- 
lages  (36)  are  somewhat  larger  and  form  longer  channel  segments, 
but  otherwise  the  two  series  belong  practically  to  the  same  develop- 
mental stage,  in  spite  of  their  difference  in  total  length  measure. 
The  correspondence,  for  example,  between  figs.  254  (series  143) 
and  259  (series  258)  is  remarkable. 

On  the  other  hand  the  majority  of  16  mm.,  16.5  mm.  and  17  mm. 
embryos  offer  decided  advances  in  the  lymphatic  development  of 
this  region  beyond  that  normally  found  in  the  15  mm.  and  15.5 
mm.  stages. 

Two  successive  sections  of  a  typical  16  mm.  embryo  (series  96) 
in  the  azygos  area  are  shown  in  figs.  261  and  262,  and  fig.  193 
gives  the  ventral  view  of  the  reconstruction  of  the  same  embryo, 
in  which  the  level  of  figs.  261  and  262  is  indicated  by  the  line  A-B. 

Comparison  with  the  immediately  preceding  series  (143  and 
258)  will  show  that  the  following  fundamental  changes  have  oc- 
curred in  the  azygos  venous  and  lymphatic  systems : 

I.  The  two  azygos  veins  (3  and  6)  have  become  reduced  in  size. 
At  the  level,  at  which  the  sections  of  figs.  261  and  262  are  taken, 
both  veins  now  lie  dorsal  to  the  intercostal  arteries  (2),  whereas  in 
the  earlier  stages  (e.g.  figs.  260,  258,  257)  the  azygos  trunks  are 
ventral  to  the  arteries,  and  the  interval  between  the  latter,  along  the 
dorsal  aspect  of  the  aorta,  is  occupied  by  the  supracardinal  inter- 
azygos  plexus. 

Reference  to  the  reconstruction  of  series  96  (fig.  193) 
shows  that  this  topographical  readjustment  has  occurred  in  the 
caudal  part  of  the  azygos  area,  below  the  level  A-B,  by  the  longi- 
tudinal hydrostatic  definition  of  the  main  supracardinal  azygos 


142       DEVELOPMENT    OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

trunks  through  confluence  of  elements  of  the  preceding  interazy- 
gos  plexus.  The  original  post-cardinal  azygos  veins,  which  in 
series  258  and  143  are  seen  to  form  the  main  channels  ventral  to 
the  intercostal  arteries,  are,  in  the  caudal  region  of  series  96, 
represented  by  two  slender  longitudinal  trunks,  on  the  lateral 
aspect  of  the  thoracic  ducts  between  them  and  the  sympathetic 
nerves  (1).  The  main  azygos  veins  have  developed  as  distinct 
circumscribed  axial  channels  out  of  the  antecedent  supracardinal 
interazygos  plexus,  dorsal  to  the  intercostal  arterial  branches  (2) . 
Correlated  with  this  new  azygos  development  is  the  reduction  of 
the  earlier  postcardinal  channels,  ventral  to  the  intersegmental 
arteries,  and  their  topographical  replacement  in  large  part  by  the 
right  and  left  thoracic  ducts  (36}  (not  labelled  in  fig.  193). 
Cephalad  of  the  level  A-B  the  reconstruction  shows  the  earlier 
relation  t)f  the  azygos  trunks,  ventro-lateral  to  the  intercostal 
arteries.  In  ascending  the  left  azygos  vein  gradually  diminishes, 
while  conversely  the  vessel  of  the  right  side  increases  in  caliber. 

II.  The  individual  separate  lymphatic  anlages  of  the  azygos 
segment  of  the  thoracic  duct  of  the  preceding  stages  have  united 
into  a  continuous  and  uninterrupted  lymphatic  channel. 

Caudad  of  the  level  A-B  (fig.  193)  the  right  and  left  thoracic 
ducts  are  fairly  symmetrical  bilateral  channels,  connected  with 
each  other  by  several  broad  and  by  a  larger  number  of  slender 
transverse  anastomoses.  They  occupy  the  position  of  the  earlier 
postcardinal  azygos  trunks,  before  these  shifted  to  the  supra- 
cardinal  position,  ventro-lateral  to  the  intercostal  arteries,  along 
the  medial  border  of  the  reduced  longitudinal  tributary  channel 
representing  on  each  side  the  remnant  of  the  earlier  post-cardinal 
azygos,  and  draining  dorsad  into  the  newly  established  supra- 
cardinal  azygos  line  of  each  side. 

Figs.  261  and  262  give  excellent  views  of  the  topographical 
relations  of  the  vascular  structures,  arterial,  venous  and  lym- 
phatic. Both  sections  show  the  right  and  left  thoracic  ducts  (36}, 
ventral  to  the  intercostal  arteries  (2),  the  lymphatic  cross  anas- 
tomosis between  the  two  along  the  dorsal  circumference  of  the 
aorta,  and  the  main  supracardinal  azygos  veins  (3,  6}.  Cephalad 
of  the  level  A-B  (fig.  193)  this  plexiform  anastomosis  between  the 


DEVELOPMENT  OF  THE  THORACIC  DUCT          143 

ducts  increases  in  extent,  and  the  entire  lymphatic  channel  in- 
clines, in  ascending,  to  the  left.  This,  as  previously  explained 
(cf.  supra,  p.  129),  is  due  to  the  greater  development  of  the  inter- 
mediate lymphatic  line,  along  the  ventral  aspect  of  the  interazygos 
anastomosis,  and  its  union  with  the  left  thoracic  duct  to  form  the 
plexiform  channel  of  the  adult.  The  corresponding  lymphatic 
of  the  right  side,  on  the  other  hand,  becomes  reduced  above  the 
level  A-Bj  and  only  its  cephalic  portion  persists  as  the  thoracic 
segment  of  the  right  lymphatic  duct  (47  in  fig.  193). 

The  extraintimal  lymphatic  anlages  ventral  to  the  thoracic 
ducts,  which  are  eventually  to  establish  the  connection  between 
them  and  the  mesenteric  lymphatics,  are  in  the  process  of  develop- 
ment in  series  96.  The  venous  core  (4)  and  the  replacing  peri- 
venous  lymphatic  (5)  are  shown  on  the  left  side  in  figs.  26 land 
262,  and  equivalent  segments  of  this  channel  are  seen  in  the  recon- 
struction (51  in  fig.  193).  In  other  portions  of  the  ventral  and 
ventro-lateral  periaortic  mesoderm  numerous  independent  inter- 
cellular spaces  begonging  to  the  same  system  are  developing. 

While  the  thoracic  ducts  are  in  the  majority  of  16  mm.  embryos 
complete  continuous  and  definite  channels,  as  in  the  present  aver- 
age example,  the  acquisition  of  this  final  condition  is  not  infre- 
quently delayed  considerably  beyond  this  period.  I  have  a  number 
of  16  and  16.5  mm.  embryos  in  which  the  thoracic  duct  develop- 
ment has  not  advanced  beyond  the  stage  typical  of  the  average 
14  mm.  or  15  mm.  embryo.  This  is  another  example  of  the  con- 
siderable range  of  chronological  variation  of  lymphatic  develop- 
ment in  individual  embryos  encountered  in  examining  a  large 
number  of  series  of  about  the  same  length  measure. 

The  16  mm.  embryo  again  furnishes  conclusive  evidence  as  to 
the  secondary  character  of  the  mutual  relation  between  embryonic 
venous  and  lymphatic  vessels,  and  shows,  in  typical  individuals, 
the  final  stage  of  the  process  through  which  temporary  venous 
channels  are  replaced  by  the  permanent  components  of  the  lym- 
phatic system.  -This  replacement,  as  demonstrated  by  the  suc- 
cessive series  of  sections  from  the  azygos  region  just  considered,  is 
a  gradual  process.  The  lymphatic  channel  has  its  inception  in 
numerous  small  extraintimal  mesenchymal  spaces  which  form 


144      DEVELOPMENT    OF    THE    SYSTEMIC    LYMPHATIC    VESSELS 

along  and  around  the  components  of  an  atrophying  embryonic 
venous  plexus,  or  follow  part  of  the  circumference  of  a  more  definite 
early  venous  trunk.  As  these  spaces  increase,  enlarge  and  become 
confluent  to  form  longer  segments  of  the  lymphatic  channel,  the 
related  venous  element  continues  to  recede,  until,  in  certain  areas, 
it  is  entirely  replaced  by  the  lymphatic  vessel.  In  other  districts, 
along  embryonic  veins  which  are  carried  into  the  adult  organiza- 
tion, as  permanent  components  of  the  venous  system,  the  redun- 
dant vein  of  the  earlier  stages  becomes  more  circumscribed  and 
more  clearly  defined  as  the  companion  lymphatic  channel  develops 
in  the  perivenous  area.  In  either  case  the  complete  or  partial 
replacement  of  venous  by  lymphatic  elements  does  not  occur 
suddenly,  but  is  accomplished  by  gradual  and  progressive  onto- 
genetic  stages.  I  can  find  no  evidence  at  any  point  of  the  separa- 
tion of  portions  of  a  venous  plexus  or  of  an  already  organized 
venous  channel,  such  detached  parts  then  uniting  directly  with 
each  other  to  form  systemic  lymphatic  vessels.  In  every  region 
of  the  mammalian  embryo  the  above  described  extraintimal 
development  of  the  lymphatic  elements,  and  the  subsequent 
secondary  topographical  replacement  of  decadent  veins  by  them, 
can  clearly  be  demonstrated.  This  process,  of  course,  leads  to  a 
stage  in  which  the  advancing  development  of  the  lymphatic  and 
the  correlated  regression  of  the  associated  venous  components 
are  balanced,  and  in  which  both,  proceeding  in  opposite  genetic 
directions,  are  found  side  by  side  in  the  same  field.  The  stages 
previously  discussed  in  detail,  between  13  mm.  and  15  mm.  offer 
abundant  illustration  of  this  intermediate  stage  in  the  azygos 
area. 

It  is  to  be  noted  that  in  the  earlier  stages  (13  to  14  mm.)  the 
lymphatic  extraintimal  spaces  first  appear  on  the  lateral  aspect 
of  the  atrophying  venules  of  the  ventro-medial  azygos  plexus,  and 
subsequently  surround  them.  They  are  then  situated  at  some 
distance  ventral  to  the  main  azygos  trunks.  In  the  later  stages 
(15  mm.,  15.5  mm.  and  16  mm.  embryos)  they  have  extended 
dorsad  and  lie  in  close  apposition  to  the  ventral  and  ventro-medial 
circumference  of  the  larger  veins,  which  position  they  maintain 
subsequently  in  their  further  development.  Coincident  with  this 


DEVELOPMENT   OF   THE    THORACIC    DUCT  145 

relative  change  in  position  of  the  earlier  lymphatic  spaces  is  the 
appearance  of  additional  thoracic  duct  anlages,  which  develop 
as  extraintimal  lymphatic  elements  along  those  lines  of  the  em- 
bryonic azygos  system  which  are  destined  to  undergo,  in  the 
later  stages,  still  further  reduction  and  final  elimination  in  the 
definite  organization  of  the  adult  condition.  [Compare  on  this 
point  the  sections  of  series  96  (figs.  261  and  262)  with  those  of 
series  253  (figs.  265  to  270)]. 

One  other  fact  deserves  careful  consideration  in  analyzing  the 
development  of  the  azygos  segment  of  the  thoracic  ducts  in  stages 
between  14  mm.  and  15  mm.  In  a  certain  proportion  of  the  em- 
bryos of  this  period  the  extraintimal  replacement  of  the  earlier 
ventro-medial  azygos  plexus  in  the  cephalic  part  of  the  future 
azygos  segment  of  the  thoracic  duct  is  delayed.  In  these  cases 
peculiar  histological  pictures  are  obtained  in  this  area.  The  com- 
ponents of  the  ventro-medial  azygos  plexus  have  become  detached 
from  the  main  veins,  and  have  fused  together  into  an  elongated 
spindle  shaped  bag,  completely  filled  with  blood,  beginning  and 
ending  blindly  and  not  in  communication  with  any  venous  channel. 
This  structure,  when  found,  invariably  occupies  the  site  of  the 
long  lymphatic  segment  seen  in  the  reconstruction  of  series  214 
(fig.  190)  on  the  right  side,  in  the  areas  A  and  B  (slides  xiv  and 
xv),  ventral  to  the  right  intercostal  arteries,  in  the  interval 
between  aorta  and  right  azygos  vein.  The  appearance  presented 
by  it  on  section  is  shown  in  figs.  263  and  264  in  a  14  mm.  cat 
embryo  (series  211,  slide  xii,  sections  2  and  8,  X  225).  It  is 
indicated  in  these  figures  by  the  leader  34,  as  a  detached  and  con- 
fluent part  of  the  original  ventro-medial  azygos  plexus.  Fig.  263 
shows  this  structure  in  the  interval  between  the  intercostal  arter- 
ies. Fig.  264  gives  a  typical  view  of  it  at  the  level  of  one  of  the 
right  intercostal  branches.  It  lies  ventral  to  the  same,  between 
aorta  (7)  mesad,  the  right  azygos  trunk  (3)  laterad,  dorsal  to  the 
oesophagus  (8).  The  blood  cells,  which  completely  fill  its  lumen, 
differentiate  from  those  circulating  in  the  continuous  vein  channels 
by  remarkably  intense  reaction  to  the  Orange-G  stain.  As 
stated,  this  structure  is  completely  detached  from  all  adjacent 
veins,  can  be  followed  cephalad  and  caudad  through  many  sec- 


146      DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC   VESSELS 

tions,  and  ends  blindly  at  either  end  in  a  gradually  diminishing 
pointed  extremity.  In  a  reconstruction  of  this  embryo  it  would 
correspond  absolutely  in  extent  and  relations  to  the  long  lym- 
phatic channel  above  referred  to  on  the  right  side  of  series  214 
(fig.  190).  A  comparison  of  the  reconstruction  (fig.  190)  and  of  the 
corresponding  sections  (figs.  214  to  240)  of  this  latter  embryo, 
clearly  reveal  the  significance  of  this,  at  first  sight,  somewhat 
anomalous  and  puzzling  structure.  It  will  be  noted  that  the  recon- 
struction of  series  214  (fig.  190)  shows,  at  the  level  of  the  line  C, 
the  caudal  end  of  a  large  ventro-medial  tributary  trunk  (34)  of 
the  right  azygos  vein  (3),  which,  in  proceeding  cephalad,  becomes 
imbedded  in  the  centre  of  the  long  extraintimal  lymphatic  chan- 
nel. The  continuation  of  this  venous  tributary  line,  detached 
from  the  functional  veins,  furnishes  the  central  venous  core  (4) 
which  is  surrounded  by  the  extraintimal  lymphatic  space  (5}  in 
all  the  sections  of  series  214  shown  in  figs.  214  to  240  inclusive. 
If  this  ventro-medial  tributary  trunk  (84  in  fig.  190)  had  organized 
in  its  entire  length,  by  confluence  of  the  radicles  of  the  preceding 
plexus,  and  had  then  become  detached  from  the  functional  right 
azygos  vein,  it  would,  before  extraintimal  development  of  the 
surrounding  lymphatic  spaces  began,  present  exactly  the  condi- 
tions seen  in  series  211.  In  comparing,  therefore,  these  two  14 
mm.  embryos,  we  find  in  series  214  the  venous  line,  around  which 
this  important  segment  of  the  thoracic  duct  develops  and  which  it 
subsequently  replaces,  present  in  the  condition  typical  for  the 
average  embryo  of  this  period,  as  a  detached  and  nearly  empty 
venous  bag,  surrounded  by  the  extraintimal  lymphatic  channel. 
On  the  other  hand,  series  211  shows  the  same  tributary  trunk,  also 
detached  from  the  main  vein,  but  still  filled  with  blood,  while  the 
enveloping  extraintimal  lymphatic  anlages  have  not  yet  made 
their  appearance.  Comparison  with  the  reconstruction  and  with 
the  sections  of  series  214  prove  its  identity  with  the  latter's  venous 
core  (4)  in  the  interior  of  the  lymphatic  channel  (5). 

A  15  mm.  embryo  of  the  Princeton  embryological  collection 
(series  53),  which  I  had  the  opportunity  of  studying  through  the 
courtesy  of  Professor  McClure,  shows  conditions  identical  with 
those  just  described  in  series  211.  It  is  interesting  and  conclusive 


DEVELOPMENT  OF  THE  THORACIC  DUCT          147 

to  further  compare  in  this  respect  the  reconstruction  of  series 
214  (14  mm.  fig.  190)  with  that  of  series  143  (15.5  mm.  fig.  192). 
In  the  former  embryo  the  secondary  para-azygos  channel  of  the 
right  side  (34),  developed  by  confluence  of  components  of  the 
right  ventro-medial  azygos  plexus,  only  persists  in  its  caudal 
portion,  and  has  in  the  rest  of  its  original  extent  been  detached  and 
surrounded  by  the  extraintimal  lymphatic  channel.  On  the  other 
hand,  in  the  15.5  mm.  series  143  (fig.  192)  this  normal  process  of 
detachment  and  replacement  by  extraintimal  lymphatic  anlages 
has  been  delayed.  Fig.  192  shows  the  para-azygos  ventro-medial 
channel  (84}  as  an  extensive  tributary  trunk  of  the  right  azygos 
vein,  cephalad  of  the  level  C.  Only  a  few  areas  of  the  extrain- 
timal lymphatic  development  occur,  as  yet,  along  its  course.  Fur- 
ther development  of  these  and  their  confluence  will  produce  the 
condition  already  seen  in  the  earlier  embryo,  series  214,  which  is 
typical  for  the  average  embryo  of  the  14  mm.  stage.  Thus 
unusual  and  atypical  delay  of  lymphatic  development  occurs  in 
some  embryos  of  this  period  in  the  region  above  specified,  and  pro- 
duces a  definite  and  uniform  aberrant  picture.  The  correct 
interpretation  of  the  same  is  given  by  the  conditions  obtaining  in 
the  average  embryo  of  this  period.  I  lay  some  stress  on  the  facts 
just  described,  because  isolated  observation  of  an  instance  of  this 
character  might  readily  lead  to  the  erroneous  assumption  that  the 
detached  venous  bag  (34)  of  figs.  263  and  264  became  directly 
transformed  into  the  lymphatic  channel  of  the  thoracic  duct  occupy- 
ing in  the  later  stages  the  identical  topographical  position  and 
maintaining  the  same  relations  to  surrounding  structures.  This 
error  can  only  be  avoided  by  determining,  in  numerous  embryos 
of  this  period,  the  typical  and  average  condition  of  lymphatic 
development. 

Thus  in  the  average  16  mm.  cat  embryo  the  originally  separate 
and  independent  extraintimal  anlages  of  the  two  thoracic  ducts 
have  become  confluent,  and  form  from  this  stage  onward  usually 
a  continuous  and  uninterrupted  lymphatic  channel,  which  is  con- 
nected with  the  general  venous  system  through  the  jugular  lymph 
sac,  by  union  with  the  thoracic  duct  approach  of  the  latter. 

From  this  stage  forward  the  subsequent  growth  and  readjust- 


148      DEVELOPMENT    OF   THE    SYSTEMIC    LYMPHATIC   VESSELS 

ment  of  the  thoracic  ducts  is  merely  a  question  of  continuous 
enlargement  of  the  lymphatic  channels  at  the  expense  of  the  azy- 
gos  veins.  The  latter  recede  still  further,  while  the  former  cor- 
respondingly increase  until  the  adult  relative  condition  of  both 
systems  is  attained.  In  this  readjustment  the  thoracic  ducts 
of  the  adult  cat  acquire  for  themselves  in  large  part  the  topo- 
graphical position  occupied  in  earlier  embryonic  stages  by  por- 
tions of  the  azygos  complex.  The  method  of  this  substitution  has 
been  sufficiently  and  repeatedly  detailed  in  the  preceding  pages. 

Figs.  265  to  270  inclusive  show  the  results  in  transverse  sections 
of  the  middle  thoracic  region  in  a  19  mm.  cat  embryo  (series  253, 
slide  xxiv,  sections  9,  11,  15,  16,  17  and  18,  X  225). 

In  fig.  265  (section  9)  both  azygos  veins  are  reduced,  but  the 
right  trunk  (3)  has  maintained  itself  as  the  principal  vessel,  still 
connected  by  the  interazygos  anastomosis  (15}  with  the  very  much 
smaller  left  azygos  (6).  Ventral  to  the  veins,  on  each  side  of  the 
aorta  (7),  are  the  right  and  left  thoracic  ducts  (36).  The  right 
duct,  as  is  invariably  the  case  in  this  region,  is  the  larger,  and  shows 
a  pointed  dorso-medial  extension  which  passes  behind  the  aorta 
towards  the  ventral  aspect  of  the  interazygos  anastomosis.  This 
is  a  further  development  of  the  same  conditions  seen  in  the  15.5 
mm.  and  17  mm.  embryos,  in  figs.  254, 255  and  259,  and  is  responsi- 
ble for  the  formation  of  the  intermediate  dorsal  lymphatic  ele- 
ment seen  in  the  16  mm.  embryo,  (figs.  261  and  262)  behind  the 
aorta,  between  the  azygos  veins  and  the  intercostal  arteries. 
(cf.  especially  left  side  of  fig.  262). 

On  the  left  side  of  fig.  265,  ventral  to  the  left  thoracic  duct,  is 
seen  a  venous  radicle  (4)  in  relation  to  an  extraintimal  anlage  (5) . 
In  section  11  (fig.  266)  this  space  has  enlarged.  In  the  succeeding 
sections  15,  16,  and  17  (figs.  267,  268  and  269)  the  same  structure 
appears  as  a  well  developed  lymphatic  channel  (51),  in  the  root 
of  the  dorsal  mesentery,  and  in  section  18,  (fig.  270)  it  opens  into 
the  left  thoracic  duct.  It  marks  one  of  the  points  of  connection 
of  the  mesenteric  lymphatic  plexus  with  the  thoracic  duct,  which 
leads  to  the  ultimate  differentiation  of  the  postazygos  segment  of 
this  channel.  The  anlage  is  the  same  previously  noted  in  the  16 
mm.  embryo,  (4  and  5,  in  figs.  261  and  262,  series  96),  and  in  the 
15.5.  mm.  embryo,  series  143  (51  in  figs.  257  and  258). 


DEVELOPMENT    OF    THE    THORACIC    DUCT  149 

Fig.  266  (section  11)  is  taken  at  the  level  of  a  pair  of  intercostal 
arteries  (2),  which  perforate  the  interazygos  anastomotic  plexus 
(15)  and  separate  the  same  from  the  azygos  trunks.  The  dorso- 
medial  extension  of  the  right  thoracic  duct  towards  the  interval 
between  the  interazygos  channel  (15)  and  the  dorsal  circumference 
of  the  aorta  (7)  has  increased.  In  section  15  (fig.  267)  it  has 
crossed  to  the  mesal  side  of  the  right  intercostal  artery  and  occu- 
pies part  of  the  area  filled  in  the  preceding  sections  by  the  inter- 
azygos anastomosis.  This  latter  is  reduced  to  insignificant 
remnants.  The  left  azygos  vein  (6)  appears  as  a  minute  channel 
between  the  left  intercostal  artery  (2)  and  the  left  thoracic  duct 
(86).  It  can  be  traced  in  the  same  condition  in  the  succeeding 
sections. 

In  sections  16,  17  and  18,  (figs.  268,  269  and  270)  the  inter- 
mediate lymphatic  channel  appears  along  the  dorsal  circumfer- 
ence of  the  aorta,  between  the  intercostal  arteries,  which  now 
pass  through  meshes  separating  the  three  chief  channels  of  the 
lymphatic  plexus,  viz.  the  left  and  right  thoracic  ducts  and  the 
intermediate  supra-aortic  lymphatic. 

The  three  last  figures  of  this  series  show  very  clearly,  by  com- 
parison with  figs.  261  and  262,  the  advances  in  lymphatic  devel- 
opment, and  the  recession  of  the  azygos  system,  especially  of  the 
left  azygos  vein,  in  passing  from  the  16  mm.  (series  96)  to  the  19 
mm.  stage  (series  253).  The  latter  presents  practically  adult 
conditions  in  both  the  venous  and  the  lymphatic  systems. 

It  only  remains  to  be  noted  that,  in  the  adult  cat,  the  right  azy- 
gos vein  shifts  secondarily  dorsad  to  a  submuscular  prevertebral 
anastomotic  venous  chain  at  the  9th  or  10th  costo-vertebral  level, 
and  thus  affords  the  opportunity  for  the  greater  development  of 
the  caudal  part  of  the  right  thoracic  duct  which  replaces  the  origi- 
nal azygos  channel  and  establishes  connection  with  the  abdominal 
lymphatics,  forming  the  above  defined  "Post-azygos  segment  of 
the  thoracic  duct." 

It  is  not  the  purpose  of  the  present  paper  to  enter  into  the 
development  of  the  abdominal  connections  of  the  thoracic  ducts. 
This  subject  requires  a  minute  consideration  of  the  conditions 
encountered  in  the  adult  mammal,  and  is  hence  properly  reserved 
for  future  detailed  consideration. 


150      DEVELOPMENT   OF   THE    SYSTEMIC    LYMPHATIC    VESSELS 

Junction  of  azygos  and  preazygos  segments  of  the  thoracic  duct 

These  segments  of  the  main  adult  lymphatic  channel  usually 
unite  by  end-to-end  fusion  in  embryos  between  15  mm.  and  16 
mm.  crownrump  measure,  although,  as  previously  stated,  the 
establishment  of  a  continuous  lymphatic  channel  may  be  delayed 
in  individual  instances  beyond  this  period. 

Figs.  271  to  275  inclusive  show  five  successive  transverse  sec- 
tions of  this  junctional  area  of  the  two  segments  in  the  cephalic 
portion  of  the  dorsal  mediastinal  region  in  a  15.5  mm.  cat  embryo 
(series  143,  slide  xii,  sections  22,  23,  24,  25  and  26,  X  200). 

Fig.  271  (section  22)  contains  the  right  precava  (3)  and  the  left 
azygos-Cuvierian  arch  (6),  with  the  cephalic  termination  of  the 
interazygos  plexus  (15,)  dorsal  to  the  oesophagus  (8).  The  caudal 
extremity  of  the  preazygos  segment  of  the  thoracic  duct  (35)  is 
seen  on  the  left  side,  and  continues  in  the  next  section  (fig.  272)  as 
the  link  between  the  preazygos  and  azygos  segments  of  the  duct 
(35,  36  in  fig.  272).  In  the  following  section  24  of  this  slide  (fig. 
273)  the  darker  area  dorsal  to  the  lymphatic  channel  marks  the 
blind  cephalic  end  of  the  left  azygos  arch,  and  hence  characterizes 
the  lymphatic  channel  (36)  as  the  beginning  of  the  azygos  por- 
tion of  the  duct.  In  fig.  274  (section  25)  the  left  azygos  arch 
(dorsal  3)  is  opened  by  the  section  and  receives  the  terminal  of 
the  cephalic  end  of  the  interazygos  plexus  (15)  seen  in  the  three 
immediately  preceding  sections  (sections  24,  23,  and  22,  figs. 
273,  272  and  271) .  We  are  therefore  now  at  the  cephalic  end  of  the 
azygos  segment  of  the  thoracic  duct  (36),  ventral  to  the  azygos 
vein  (3)  and  the  interazygos  anastomosis,  and  can  trace  the  same 
uninterruptedly  from  this  point  cephalad  into  continuity  with  the 
beginning  of  the  preazygos  channel  (35),  as  seen  in  sections  23  and 
22,  figs.  272  and  273. 

In  the  following  section  (26,  fig.  275)  the  left  azygos  arch  (3) 
is  fully  opened,  in  its  turn  ventrad  to  join  the  left  precaval  vein, 
and  the  azygos  segment  of  the  thoracic  duct  (36)  occupies  the 
typical  position  of  this  period,  between  the  ventro-medial  aspect  of 
the  right  azygos  trunk  (3)  and  the  dorso-lateral  circumference  of 


DEVELOPMENT  OF  THE  THORACIC  DUCT          151 

the  oesophagus   (8),   trending  sinistro-cephalad  into  the  line  of 
the  preazygos  segment  (35,  in  figs.  271  and  272). 

Reference  to  the  dorsal  view  of  the  reconstruction  of  this  em- 
bryo (fig.  171)  shows  that  the  azygos  segment  of  the  thoracic 
duct  (36)  has  united  with  part  of  the  caudal  division  of  the  preazy- 
gos chain  of  lymphatics  (35),  cephalad  of  the  interazygos  anasto- 
mosis, into  a  continuous  lymphatic  channel,  although  the  con- 
tinuity with  the  main  preazygos  segment  has  not  yet  been  com- 
pletely established.  In  other  words  this  condition  has  been  very 
nearly,  but  not  quite,  attained.  Some  of  the  preazygos  elements 
(35}  have  already  fused  with  the  azygos  segment,  thus  carrying 
the  latter  cephalad  beyond  the  interazygos  anastomosis  into  the 
territory  of  the  preazygos  portion  of  the  thoracic  duct. 


PART  II,  PLATES 

FIGURES  194  TO  275 


FIGURES  194  AND  195 

194  Transverse  section  of  middle  thoracic    region  of    11    nun.  cat    embryo; 
(series  213,  slide  XI,  section  9)  X  225. 

195  Same,  section  10. 

1  Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

34    Ventro-medial  azygos  plexus. 


THE  .SYSTEMIC1   LYMPHATIC   VESSELS 


PLATE   106 


<»     •!•-.  »';-    -   -,       *•»> 

BSSff^KrVrS 


195 


MEMOIR    NO.    1,   HUNTINGTON,    1911 


FIGURES  196  AND  197 

196  Same,  section  27. 

197  Same,  section  29. 

1  Sympathetic  nerve. 

2  Intercostal  artery. 

3  Right  azygos  vein,  thoracic  portion. 
6  Left  azygos  vein,  thoracic  portion. 

34    Ventro-medial  azygos  plexus. 


PLATE  107 


WWv* 


.  -'!/•    * 


\»  '^^  ^      """fe  *r  *~fc  A?V          *^%  ^j  A^  * 

^ty>j*»-^*/  S^r^i-  ^*^*J5 
*kj.  /..jfiL,*,****  ^^"iLi^C.l  %  ^ 

k &. T^*W% ™ ^^-^ ,^/ar  *. .<fc1i\y  **  .  ^B'.^^  -.*    -  _    •**»  ,*°** 


197 

nTU      XTU         1         TTTTTVTTT  VnT/^  V         1Q1   1 


FIGURES  198  AND  199 

198  Transverse    section  of    middle  thoracic  region  of  12  mm.  cat  embryo, 
(series  217,  slide  XI,  section  27 (  X  225. 

199  Same,   section  28. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

34    Ventro-medial  azygos  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


-±/^rf7Z-  vtw?m 

•  ••      JfEfy  '  ',ii.T.»-i;--; .,;.' 

^^m^/m 

f  &  '^V-.. *  *  >«  V,^*  ' 

*»  "*~^y^    *  iCJ  "A.  * » '"£i*'t'.'> 


<?^^  W  v?5S 


34 


199 


MEMOIR   NO.    1,    HUNTINOTON,   1911 


FIGURES  200  AND  201 

200  Sanie,  section  2l>. 

201  Same,  slide  X,  section  18. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygofi  vein,  thoracic  portion. 

7  Aorta. 

34    Ventro-medial  azygos  plexus. 


THE   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE   109 


^^^§f^^s 


201 


MEMOIR   NO.   1,   HUNTINGTON,    1911 


FIGURES  202  AND  203 

202  Same,  section  30. 

203  Same,  section  31. 

1     Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior^of  develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degener- 

ating embryonal  vein. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

34     Ventro-medial  azygos  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  110 


k?'*>-:.;\^'    ,     •'»"-          ~ 

w£*i$#&4ss  ,  "  ^  x 

W$j&^ 

>',  i  &•  -  k-~,  <.  „-«     ^.  „ 

i.      >fl'  -?    v*  •• 

^x^x 
I'j-i^* 

'^«^p 

itiiJS^ 


FIGURES  204  AND  205 

204  Transverse  section  through  middle  thoracic:  region  of    a  13.5  mm.   cat 
embryo;  (series  189,  slide  X,  section  15)  X  225. 

205  Same,  section  16. 

1  Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  ve.n,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

34     Ventro-medial  azygos  plexus. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


205 


MKMOIR    NO.    1,   HUNTINGTON,    1911 


FIGURES  206  AND  207 

206    Transverse    section  through  middle  thoracic  region    in  a    13.5  mm.  cat 
embryo,  (series  76,  slide  XI,  section  15)  X  300. 
'  207      Same,    section    16. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degener- 

ating embryonal   vein 

7  Aorta. 

8  Oesophagus. 

15     Interazygos  venous  plexus. 


THE  SYSTEMIC   LYMPHATIC   VESSELS 


PLATE    112 


V  -jsaaJX1^      r*<yhlfc>? 

'&Z#ti£& 


207 


MEMOIR   NO.    1,   HTJNTINGTON,    1911 


FIGURES  208  AXD  209 

20S    Same,  section  17. 
209    Same,  section  19. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  develop- 

ing and  replacing  lymphatic  vein. 

5  Extraintimal  or  perivenous  lymphatic   space  surrounding  degener- 

ating embryonal  vein. 
(3    Left  azygos  vein,  thoracic  position. 

7  Aorta. 

8  Oesophagus. 

15     Interazygos  venous  plexus. 


THK   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE   113 


r ;-;,.- ''-•.:•••.  wK*' 
v ''frt-'-'-'V.-v'vcK 

XT.    ,  .:.v--.le    •.. 


209 


MEMOIR  NO.   1,   HUNTINGTON,    1911 


FIGURES  210  AND  211 


210  Same,  section  21. 

211  Same,  section  22. 


1     Sympathetic  nerve. 

3     Right  azygos  vein,  thoracic  portion. 


4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degener- 

ating embryonal  vein. 

7  Aorta. 

8  Oesophagus. 

15     Interazygos  venous  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


li  *   *%      ^^  '%**«*»   «  "~ '  ^~*     '•"  '.^B        ^          ^    "*     *X^         *" 

^^ 


210 


211 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  212  AND  213 

212  _  Same,  section  23. 
213.f  Same,  section  28. 

1    Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

15     Interazygos  venous  plexus. 


PLATE   115 


212 


: 


213 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  214  TO  217 

214  Transverse    section    through    middle  thoracic    region  in  a  14  mm.  rcat 
embryo,  (series  214,  slide  XIV,  section  15)  X  225. 

215  Same,  section  16. 

216  Same,  section  17. 

217  Same,  section  19. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  sourrounding  degenerat- 

ing embryonal  vein. 


PLATE  116 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


MEMOIR   NO.    1,   HtTNTINGTON,    1911 


FIGURES  218  TO  221 

218  Same,  section  20. 

219  Same,  section  22. 

220  Same,  section  26. 

221  Same,  section  27. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   117 


/Ssfe^W* 


218 


219 


220 

MEMOIR    NO.   1,   HUNTINGTON,    1911 


221 


FIGURES  222  TO  225 

222  Same,  section  28. 

223  Same,  section  32. 

224  Same,  section  34. 

225  Same,  section     1. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerat- 

ing embryonal   vein. 

6  Left  aeygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

16     Interazygos  venous  plexus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   118 


222 


223 


p^^SP* 

^ 


^^^mm 

•;••„     V-^v   >ilV-V.*ty&3 

*       ^•'.--tX         ,V,Ofc  '-*4*    »WV  *. %?  ^ 


224 

MEMOIR   NO.    1,   HUNTINGTON,    1911 


225 


FIGURES  226  TO  229 

226  Same,  section  2. 

227  Same,  section  3. 

228  Same,  section  4. 

229  Same,  section  5. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


&*m$& 

V-*-*.^'^^'^' .'.%••: 

VT'$ •*"•*''•'    •'•>'.»  *•'  * '*      *\ 
f*\        *  *«  «'•-„'--».   -  ?••    -V 

^u*-v  fV>»**K . ,  -  '-•  ~*  v\"x^w 

Vv    **-.  •  ?'    /•"  •»  "^"  «••  •«<* 


Hlp^«%<i»  *  •  »  *      -  v •.;,      «ix*O;-'«.1^- 

HL^5^'r  "''"^  "  ' '  *  ^S^^^&  -»  '      -^ 

S&***V-'jv^»!i(4jf  ^v? 

^&v,  «      '    »  l«v    f.  */P  ^.V- 

Mrr;-^l'        "i 


PWX        W     ^          N 

^ftPS^Sa 

«rS^-:>  '-'vl  v'-'-V.^ 

p^i^^fe: 

'^' ' ' ^fic" v / .\'V V.?  L» '•  V .     X'  • '  . 


228 

MEMOIB   NO.    1,   HUNTINGTON,    1911 


229 


FIGURES  230  TO  233 

230  Same,  slide  XV,  section  10. 

231  Same,  section  11. 

232  Same,  section  14. 

233  Same,  section  16. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 

6  Left  azygos  vein,  thoracic  postion. 

7  Aorta. 

8  Oesophagus. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE   120 


**»  '    *••.        m*     w«    *  •    -        •  <  •     r  *  fc  W    JP****    •  i 

•.*•••-•<•.  -•*:•:  £•». <-.;..««-sA.>4:..-" 

*      'V*         X"  ;r   i^Ri-v*  1-"^        ^^ 

H^k'1    - 


n  -     ."I*-,*    *  *r    ** •*   *.L*    €»"»»••* 


/SlPiSk^  •"'• 

•'">W ''  i  %:s^*^-  4  *  ••'' V 

f.tSJr  , ....y.»-     .r|>vk  ...  .»     " 


232 

MEMOIR   XO.l,   HUNTINGTON,    1911 


233 


FIGURES  234  TO  237 

234  Same,  section  19. 

235  Same,  section  21. 

236  Same,  section  27. 

237  Same,  section  28. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space  surrounding  degenerating 

embryonal  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  121 


234 


235 


236 

MEMOIR   NO.    1,  HUNTINGTON,    1911 


237 


EXPLANATION  OF  FIGURES  238,  239  AND  240 

238  Same,  section  29. 

239  Same,  section  30. 

240  Same,  section  31. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing  and 
replacing  lymphatic  space. 

5  Extraintimal   or  perivenous  lymphatic  space  surrounding    degenerating 
embryonal  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  122 


*  *       ?••.*?*    '      '*'',£.&-  v 


238 


239 


240 


MEMOIR   NO.   1,  HUNT1NGTON,   1911 


241     Transverse    section    of    lower    thoracic  region  of   14  mm.   cat     embryo 
(series  127,  slide  X,  section  3)  X  225. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

34    Ventro-medial  azygos  plexus. 


THE   SYSTEMIC   LYMPHATIC   VESSELS 


PLATE  133 


241 


MEMOIR   XO.    1,   HU.NTINOTON,    1911 


FIGURES  242  AND  243 

242  Same,  section    4. 

243  Same,  section  10. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal    or   perivenous   lymphatic    space    surrounding    degen- 

erating embryonal  vein. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 


THE   SYSTEMIC   LYMPHATIC  VESSELS 


PLATE    124 


*»  »*     ••  ""1'-.'v        "*•  JL    »         y  f'  TJV 

'"'•.:  '    ,'  •   v    ™ ,'t  >•»        .  «^  - 


243 


MEMOIR    NO.    1,    HUNTIXOTON,    1911 


FIGURES  248  TO  251 

Same,  section  19. 
Same,  section  20. 
Same,  section  21. 
Same,  section  22. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  develop- 

ing and  replacing  lymphatic  space. 

5  Extraintimal    or   perivenous   lymphatic   space   surrounding    degen- 

erating embryonal  vein. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  126 


^  ***     *".***<"      "*"^*J?*\,     *f  '    <1  /,'  'V»  '     ?*'•".'    "'•**• 


•»  £  *  '•».          «  .-  .  •     /••• 
J-1'***.:         ^v        <+ 

•;.  .'-t    ^/,W 

5-       &M$ 

/:r  .'  p4?^ 


/;  VW^^^'WB 

"••V.  .^Kr^Kl 


r.  v»    •aSW'^TTT^aftsX ,  i%^J.y^si"      /«'' 

J?' 


250 

MEMOIR   NO.    1,   HUNTINGTON,    1911 


251 


FIGURES  252  AND  253 

252  Transverse  section  though  lower  thoracic  region  of  a  15.5  mm.  cat  embryo, 
(series  143,  slide  XVIII,  section  7)  X  225. 

253  Same,    section    11. 

1  Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

34    Ventro-medial  azygos  plexus. 
36    Thoracic  duct,  azygos  segment. 


THE  SYSTEMIC   LYMPHATIC   VESSELS 


I'LATK    127 


252 


253 


MEMOIR   NO.    1,   HUNTIXGTON,    1911 


FIGURES  254  AND  255 

254  Same,  section  12. 

255  Same,  section  13. 

1  Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

36    Thoracic  duct,  azygos  segment. 


254 


255 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  256  AND  257 

256  Same,  section  14. 

257  Same,  slide  XVII,  section  31. 

1  Sympathetic  nerve. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

34     Ventro-medial  azygos  plexus. 
36    Thoracic  duct,  azygos  segment. 
51     Mesenteric  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE    129 


*$&& 

fe&3ss8 


256 


f?T*ft    V  ?• 
*L5fi3-/!  *.*« 


257 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  260  AND  261 

260  Same,  section  9. 

261  Transverse  section  of  lower  thoracic  region  in    a    16  mm.  cat  embryo, 
(series  96,  slide  XII,  section  32)  X  200. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space    surrounding   degen- 

erating embryonal   vein. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

36    Thoracic   duct,    azygos   segment. 


THE  SYSTEMTC  LYMPHATIC  VESSELS 


PLATE  131 


260 


261 


MKMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  262  AND  263 

262  Same,  section  33. 

263  Transverse  section    of    middle  thoracic  region  in  a  14  mm.  cat  embryo, 
(series  211,  slide  XII,  section  2)  X  225. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintimal  or  perivenous  lymphatic  space    surrounding    degen- 

erating embryonal  vein. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta 

8  Oesophagus. 

15     Interazygos  venous  plexus. 
34    Ventro-medial  azygos  plexus. 
36    Thoracic  duct,  azygos  segment. 


THE  8YSTEMIC  LYMPHATIC  VESSELS 


PLATE  132 


^;; 
#ffl 


34 


263 


MEMOIR   NO.    1,   HUNTINGTON,    1911 


FIGURES  264  AND  265 

264  Same,  section  8. 

265  Transverse    section  of  middle  thoracic  region  in  a  19  mm.  cat  embryo, 
(series  253,  slide  XXIV,  section  {))  X  225. 

1     Sympathetic  nerve. 

3^  Right  azygos  vein,  thoracic  portion. 

4  Atrophying  embryonal  vein,  forming  kernel  in  interior  of  developing 

and  replacing  lymphatic  space. 

5  Extraintima,!   or  perivenous  lymphatic    space    surrounding    degen- 

erating embryonal  vein. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

15     Interazygos  venous  plexus. 
34    Ventro-medial  azygos  plexus. 
36    Thoracic   duct,    azygos   segment. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  133 


264 


15 


*     -^         •<^V-r"/^V 

4^^5^^1 


.v  *      vL/  r   '.        „-"'»•%"    .-  -          \         i 

'•>«'    r;      '•"•*:—  :?^;*«^»^4    .  ^-        Vy 

^.^••:i«^^,-;-:Vl 


265 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  26<>  AND  267 


266  Same,  section  11. 

267  Same,  section  15. 


Sympathetic  nerve. 

Intersegmental    arteries. 

Right  azygos  vein,  thoracic  portion. 

Extraintimal  or  perivenous  lymphatic  space  surrounding  degen- 

erating embryonal  vein. 
Left  azygos  vein,  thoracic  portion. 
Aorta. 

Interazygos  venous  plexus. 
Thoracic  duct,  azygos  segment. 
Mesenteric  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  134 


26b 


51 


267 


MEMOIR   NO.    1,    HUNTINGTON,    1911 


FIGURES  268  AND  269 

268  Same,  section  16. 

269  Same,  section  17. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

36    Thoracic  duct,  azygos  segment. 
51     Mesenteric  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  135 


258 


269 


MEMOIR    NO.    1,    HUNTINGTON,    1911 


FIGURP;S  270  AND  271 

270  Same,  section  18. 

271  Transverse  section  of  anterior  thoracic  region  inRa  15.5  mm.  cat  embryo 
(series  143,  slide  XII,  section  22),  X  200. 

1  Sympathetic  nerve. 

2  Intersegmental  arteries. 

3  Right  azygos  vein,  thoracic  portion. 

6  Left  azygos  vein,  thoracic  portion. 

7  Aorta. 

8  Oesophagus. 

15  Interazygos  venous  plexus. 

35  Thoracic  duct,  preazygos  segment. 

36  Thoracic  duct,  azygos  segment. 
51  Mesenteric  lymphatics. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  136 


;>~£&SsEsF% 

,''•;.  .\-Hl*si;s«^^Sj 


FIGURES  272  AND  273 

272  Same,  section  23. 

273  Same,  section  24. 

1  Sympathetic  nerve. 

3  Right  precaval  vein. 

6  Left  azygos-precaval  junction. 

8  Oesophagus. 

9  Trachea. 

15     Interazygos  venous  plexus. 

35  Thoracic  duct,  preazygos  segment. 

36  Thoracic  duct,  azygos  segment. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE 


273 


MEMOIR    NO.    1,    HUXTINGTON,    1911 


FIGURES  274  AND  275 

274  Same,  section  25. 

275  Same,  section  26. 

1  Sympathetic  nerve. 

3  Right  aygos  vein,  thoracic  portion. 

3  Right  precava. 

6  Left  azygos-precaval  junction. 

8  Oesophagus. 

36  Thoracic  duct,  azygos  segment. 


THE  SYSTEMIC  LYMPHATIC  VESSELS 


PLATE  138 


'  ' 


274 


275 


MEMOIR   NO.    1,   HUXTIXGTOX, 


SUMMARY  AND  CONCLUSIONS 

In  concluding  this  part  of  the  record  of  observations  on  the  on- 
togeny of  certain  axial  systemic  lymphatic  channels  in  embryos 
of  the  domestic  cat,  I  desire  very  briefly  to  contrast  the  results  of 
this  investigation  with  the  tenets  of  the  theories  of  mammalian 
lymphatic  development  divergent  from  the  views  here  expressed. 
This  is  not  done  for  the  purpose  of  inciting  or  prolonging  a  con- 
troversial discussion.  As  far  as  I  am  personally  concerned,  con- 
troversy is  at  an  end,  because  I  believe  that  I  have  furnished  posi- 
tive evidence  of  the  correctness  of  the  opinion  which  I  have 
maintained  during  the  past  six  years,  from  the  time  on  when  my 
investigations  first  warranted  definite  conclusions.  The  results 
given  in  previous  publications,  and  more  in  detail  in  the  preceding 
pages,  afford  to  me  a  sound  basis  for  interpreting  my  findings  of 
adult  as  well  as  of  embryonic  organization  of  the  lymphatic  system 
both  in  mammals  and  in  the  other  vertebrate  classes.  Conse- 
quently, until  these  results  are  successfully  accounted  for  on  an 
equally  broad  and  phylogenetically  consistent  hypothesis  differ- 
ing from  my  own  interpretation,  and  until  the  deductions  based 
on  them  are  shown  to  be  erroneous  by  equally  full  and  compre- 
hensive proofs,  I  shall  rest  quite  satisfied  with  the  position  I  have 
reached  on  this  question. 

It  may,  however,  serve  a  useful  purpose  in  enabling  scientific 
men  in  general  to  draw  their  own  conclusions,  if  the  facts  here 
offered  are  contrasted  in  a  final  review  with  the  divergent  theories 
of  lymphatic  development  which  have  been  propounded  in  the 
last  decade. 

In  regard  to  the  view  which  supposes  the  mammalian  lymphatic 
system  to  arise  by  an  outgrowth  or  bud  from  one  or  more  sacs  of 
venous  origin  and  thence  to  extend  by  a  continuous  centrifugal 
process  from  centre  to  periphery,  terminating  in  closed  lymphatic 
capillaries,  I  find  little  to  say. 

153 


154  SYSTEMIC   LYMPHATIC  VESSELS  IN  DOMESTIC  CAT 

It  is  quite  true  that  it  is  possible  to  inject  the  jugular  lymph 
sacs  in  certain  mammalian  embryonic  stages  and  thus,  by  grad- 
ing the  preparations,  to  obtain  pictures  which  might  be  interpreted 
in  the  sense  of  this  theory,  provided  all  questions  as  to  the  onto- 
genetic  history  of  lymphatic  organization  are  designedly  left  out 
of  consideration.  There  may  be  a  royal  road  to  the  solution  of  the 
vertebrate  lymphatic  problem,  but  surely  the  injection  method 
has  not  found  it.  It  will  furnish  abundant  illustrations  of  a  pre- 
sumably progressive  extension  of  lymphatic  development  from 
centre  to  periphery,  but  no  proof  of  the  actual  occurrence  of  the 
process.  The  tissues  of  the  developing  vascular  system  in  mam- 
malian embryos  afford  at  no  period  and  in  no  region  the  slightest 
evidence  of  such  an  occurrence.  On  the  o^her  hand,  the  mammal- 
ian embryo  does  offer  conclusive  evidence  of  the  development  of 
mesenchymal  spaces,  arising  independently  of  the  veins,  and  lined 
by  a  lymphatic  endothelium  which  is  not  derived  from  a  pre-exist- 
ing haemal  endothelium.  These  spaces  form  the  anlages  of  the 
future  systemic  lymphatic  channels,  and  they  are  continuous  with 
intercellular  tissue  spaces  limited  by  the  surrounding  indifferent 
mesodermal  cells  which  have  not  yet  assumed  endothelial  charac- 
ter. This  relation  of  lymphatic  anlages/  ned  by  lymphatic  endo- 
thelium, to  the  intercellular  mesenchymal  tissue  spaces,  while 
clearly  determined  in  mammalian  embryos,  is  moreover  strikingly 
and  diagrammatically  demonstrated  in  reptilian  embryos. 

I  have  given  in  the  preceding  pages  my  reasons  for  assigning 
an  absolutely  negative  value  to  injection  experiments  in  de- 
termining lymphatic  ontogeny.  These  preparations  yield  interest- 
ing topographical  pictures  in  the  different  stages,  showing  the 
extent  of  continuous  lymphatic  organization  at  different  periods, 
but  they  do  not  touch  the  problem  of  the  genetic  processes  respon- 
sible for  the  establishment  of  a  set  of  vascular  channels  capable 
of  injection.  Much  of  the  general  confusion  of  ideas  evident  in 
discussions  of  the  question  arises,  in  my  opinion,  from  the  failure 
to  correctly  appreciate  the  value  and  significance  of  the  lymph- 
heart  remnants  of  venous  origin  wrhich  in  the  mammal  are  interpo- 
lated as  junctional  links  between  the  independently  developed 
systemic  lymphatic  vessels  and  the  permanent  functional  veins. 


SUMMARY  AND   CONCLUSIONS  155 

It  seems  difficult,  in  spite  of  carefully  chosen  expressions,  to 
make  it  clear  that  in  my  interpretation  of  mammalian  lymphatic 
ontogeny  I  am  not  trying  to  straddle  the  question  of  venous  or 
non-venous  origin  of  the  lymphatic  vessels.  What  we  ordinarily 
describe  as  'lymphatic  channels'  both  in  the  embryo  and  in  the 
adult  animal  I  am  forced,  by  the  results  of  my  investigations,  to 
regard  in  amniotes  as  vessels  developed  absolutely  independently 
of  the  haemal  vascular  system.  The  association  of  these  channels, 
in  the  mammalian  embryo,  with  certain  embryonal  venous  lines 
is  purely  a  secondary,  mechanical  and  topographical  relationship, 
expressed  by  the  condensed  term  of  '  extraintimaP  development 
of  mammalian  systemic  lymphatic  vessels,  and  absolutely  devoid 
of  genetic  significance.  This  is,  without  reference  to  other  ver- 
tebrate classes,  proved  by  the  development  within  restricted  areas 
in  the  mammalian  embryo  of  systemic  lymphatic  channels  through 
the  direct  confluence  of  intercellular  mesenchymal  clefts,  not  re- 
lated topographically  or  in  any  other  sense  to  the  embryonal  veins. 
It  is  true  that  in  the  mammal  this  independent  lymphatic  genesis 
is  extremely  limited,  and  that  the  majority  of  the  lymphatic  ves- 
sels develop  in  close  association  with  embryonal  veins,  as  products 
of  the  confluence  of  periv  lous  extraintimal  spaces.  But  this  is 
merely,  as  shown  by  comp;  rison  with  other  amniote  embryos,  the 
expression  of  the  peculiar  relations  obtaining  in  the  mammal  be- 
tween the  venous  and  lymphatic  circuits  of  the  vascular  system, 
developed  independently  of  each  other. 

On  the  other  hand,  I  am  trying  to  give  its  full  value  to  a  hitherto 
unrecognized  component  of  the  finished  lymphatico-venous 
organization  of  the  mammal.  I  am  trying  to  establish  the  ex- 
tremely reduced  and  rudimentary  mammalian  lymphatico-venous 
heart  in  the  position  which  its  phylogeny  entitles  it  to  occupy,  as 
the  link  or  bond-piece  between  vertebrate  lymphatic  and  venous 
channels.  I  desire  to  make  it  as  perfectly  clear  as  it  is  possible  to 
do  in  the  English  language  that  this  does  not  mean  the  acceptance 
of  a  mixed,  partly  venous  and  partly  independent  genesis  of  the 
lymphatic  system  as  a  whole.  It  merely  calls  for  the  morpho- 
logical recognition  of  a  distinct  and  valid  structure,  interposed,  as 
the  connecting  link,  between  the  definite  venous  channels  and  the 


156  SYSTEMIC   LYMPHATIC   VESSELS  IN  DOMESTIC   CAT 

lymphatic  vessels,  genetically  a  derivative  from  the  former,  but 
in  no  sense  responsible  for  the  development  of  the  latter.  It  is 
perhaps  possible  to  illustrate  my  meaning  by  a  comparison  drawn 
from  an  entirely  foreign  field.  The  pronephric,  and  the  subse- 
quent Wolffian  duct,  in  approaching  the  cloaca,  is  met  by  a  re- 
sponsive outgrowth  of  the  latter  and  eventually  gains  its  perma- 
nent opening  into  the  genito-urinary  cavity  by  union  with  the 
same.  Nobody  would  hold  this  cloacal  horn  responsible  for  the 
Wolffian  duct  development  by  a  process  of  'outgrowth'  of  'bud- 
ding.' The  embryonal  veins  respond  in  exactly  the  same  way  to 
the  approach  of  the  independently  developed  systemic  lymphat- 
ics. This  response  in  the  typical  and  prevalent  mammal  takes 
the  form  of  a  rudimentary  and  foreshortened  lymphatico-venous 
heart,  and  continues  to  function  as  such  throughout  the  life  of  the 
individual,  as  the  jugular  lymph  sac.  There  is  here  certainly  a 
distinct  genetic  principle  involved.  We,  to  a  certain  extent,  dis- 
regard the  cloacal  participation  in  the  final  establishment  of  the 
Wolffian  duct  connection  with  the  genito-urinary  sinus,  because 
the  ontogeny  of  the  duct  in  itself  presents  such  marked  and  strik- 
ing stages.  In  exactly  the  same  general  way  I  believe  that  we  are 
prone  to  misinterpret  the  vertebrate  lymphatico-venous  junctions, 
unless  we  recognize  lymphatico-venous  hearts  and  their  remnants 
in  their  true  morphological  significance,  as  links  uniting  struc- 
tures genetically  distinct  and  of  different  origin.  In  the  matter 
here  under  discussion  this  does  not  mean  a  double  genesis  for  the  lym- 
phatic vessels,  part  derived  from  the  veins,  part  by  independent 
mesenchymal  confluence  of  intercellular  spaces.  This  would  be 
no  more  in  accordance  with  the  actual  facts  than  a  genetic  de- 
scription ascribing  a  portion  of  the  Wolffian  duct  to  cloacal  '  out- 
growth,'while  another  portion  is  credited  to  independent  develop- 
ment. I  would  refrain  from  laying  stress  on  these  facts  were 
they  based  on  guess-work,  but  the  entire  genetic  history  of  lym- 
phatic and  venous  organization  in  all  amniote  types  heretofore 
examined  is  so  strikingly  consistent  and  so  uniformly  constant 
that  my  personal  conviction  of  the  truth  of  the  above  statements 
is  very  firmly  rooted. 


SUMMARY  AND   CONCLUSIONS  157 

Observations  made  on  vascular  structure  and  growth  in  the 
transparent  tails  of  living  anure  amphibia  have  of  late  been 
offered  in  support  of  the  theory  of  continuous  centrifugal  lym- 
phatic development  from  pre-existing  venous  endothelium.  These 
observations  recall  vividly  the  corresponding  historical  period 
in  the  developmental  analysis  of  the  embryonic  blood-vascular 
channels,  prior  to  Thoma's  classical  researches  on  this  subject. 
Sigmund  Mayer  nearly  thirty  years  ago  employed  the  tails  of 
living  anure  larvae  for  the  purpose  of  studying  this  phase  of  the 
circulatory  system.  It  seems  strange  that  to-day  it  should  be 
equally,  or  even  more,  difficult  to  induce  observers  to  differentiate 
between  development  and  growth  of  vascular  channels.  Develop- 
ment means  the  genesis  of  the  first  embryonic  anlages  of  a  vascular 
system.  When  this  has  once  been  established  its  further  exten- 
sion by  growth  is  an  entirely  different  problem  which  demands 
equally  careful  and  competent  observation  and  presents  many 
phases  difficult  of  interpretation,  involving,  among  others,  the 
entire  question  of  the  'specificity  of  vascular  endothelium.' 
Much  futile  and  controversial  discussion  could  be  avoided  if 
the  growing  generation  of  contributors  to  this  subject  will  re- 
strain their  enthusiasm  long  enough  to  bear  this  vital  difference 
in  mind. 

On  the  other  hand,  the  theory  which  regards  the  lymphatic 
channels  of  the  mammalian  embryo  as  developing  by  the  coa- 
lescence of  multiple  venous  'outgrowths'  or  portions  of  embryonic 
venous  plexuses,  detached  and  separated  secondarily  from  the 
parent  veins,  deserves  detailed  consideration. 

According  to  the  postulates  of  this  view,  the  lymphatic  endo- 
thelium is  the  direct  descendant  of  the  pre-existing  haemal  vascu- 
lar endothelium  lining  the  detached  venous  elements  which  enter 
into  the  formation  of  the  lymphatic  channels.  The  latter,  after 
being  thus  established,  make  secondary  and  permanent  connec- 
tions with  the  venous  system. 

It  is  of  course  a  very  easy  matter  to  prove  in  successive  stages 
the  topographical  correspondence  of  venous  and  lymphatic  chan- 
nels, to  prove,  in  other  words,  that  the  area  occupied  by  a  vein  in 
the  earlier  stages  is  filled  in  the  following  periods  by  a  lymphatic 


158  SYSTEMIC  LYMPHATIC  VESSELS  IN  DOMESTIC  CAT 

channel.  The  genetic  succession  of  mammalian  lymphatic  ves- 
sels, developing  along  and  around  atrophying  antecedent  embry- 
onal veins  and  eventually  replacing  them  absolutely  in  the  topo- 
graphical sense,  has  been  sufficiently  elaborated  in  the  preceding 
pages.  There  is  no  question  whatever  concerning  the  anatomical 
fact  of  such  replacement.  My  quarrel  lies  with  the  deductions 
which  the  sponsors  of  the  theory  just  quoted  draw  from  the  evi- 
dence of  their  slides. 

If  in  an  earlier  stage  they  find  a  vein  or  venous  radicle  occupy- 
ing a  definite  and  clearly  circumscribed  topographical-position  in 
relation  to  surrounding  structures,  and  if  they  encounter  in  a  later 
stage  a  lymphatic  channel  in  the  identical  position  of  the  earlier 
vein,  they  reason  that  this  topographical  coincidence  proves 
the  direct  transformation  of  the  preceding  vein  into  the  succeed- 
ing lymphatic.  They  speak  of  the  earlier  vein  as  an  '  outgrowth' 
from  the  main  venous  channel  and  describe  the  same  as  being  '  de- 
tached' or  'split  off'  the  latter  to  form  a  Veno-lymphatic  anlage,' 
which  then,  by  fusion  with  multiple  equivalent  detached  venous 
elements,  forms  finally  a  valid  and  permanent  systemic  lymphatic 
channel.  It  appears  to  me  that  in  this  process  of  reasoning  topog- 
raphy is  forced  to  substitute  for  histogenesis,  and  that  the  vital 
intermediate  genetic  stages,  which  finally  produce  the  result  under 
discussion,  have  been  disregarded.  I  believe  that  this  error  in 
deduction  is  based  on  perfectly  correct  but  insufficient  premises 
and  is  due  to  the  lack  of  sufficient  material  capable  of  demonstrat- 
ing the  intermediate  histogenetic  stages  through  which  the  replace- 
ment of  a  venous  by  a  lymphatic  channel  is  accomplished.  There 
are  many  individual  embryos  of  certain  stages,  which,  interpreted 
by  themselves,  tend  to  support  strongly  the  hypothesis  of  direct 
conversion  of  venous  into  lymphatic  anlages.  It  requires  a  very 
large  number  of  embryos  of  approximately  the  same  age  in  order 
to  demonstrate  the  true  genetic  processes  governing  the  early- 
relations  of  the  venous  and  lymphatic  channels  in  the  mammalian 
embryo.  Hence  the  futility  of  reasoning,  from  a  few  human  em- 
bryos, concerning  primate  lymphatico-venous  relations,  which 
we  know,  from  the  already  ascertained  conditions  in  adult  platyrrh- 
ine  and  catarrhine  forms,  present  one  of  the  most  complicated 


SUMMARY  AND   CONCLUSIONS  159 

and  involved  problems  in  the  entire  genetic  history  of  mammalian 
vascular  organization. 

I  am  convinced  that  the  theory  of  direct  derivation  of  the  mam- 
malian systemic  lymphatic  vessels  from  the  embryonal  veins  is 
utterly  wrong  and  that  it  is  based  primarily  on  insufficient  obser- 
vation. It  lends  itself  to  an  easy  interpretation  of  a  relatively  small 
number  of  mammalian  embryos  of  each  appropriate  stage,  but 
fails  utterly  in  reckoning  with  the  conditions  presented  by  a  large 
consecutive  series  of  the  critical  periods. 

I  will  analyze  this  view  on  the  basis  of  the  material  discussed 
in  the  preceding  pages,  first  in  the  region  of  the  thoracic  duct  ap- 
proach of  the  jugular  lymph  sac  and  in  the  preazygos  segment 
of  the  thoracic  duct,  and  subsequently  in  the  azygos  district  of  the 
latter. 


I.  THORACIC  DUCT  APPROACH  AND  PREAZYGOS  SEGMENT  OF  THE 

THORACIC  DUCTS 

The  terminal  portion  of  the  thoracic  duct  has  been  described 
as  developed  by  confluence  of  venous  outgrowths,  arising  along 
the  dorsal  surface  of  the  left  common  jugular  and  innominate  veins 
in  the  earlier  (14  mm.)  stages,  which  occupy  the  same  relative 
position  with  respect  to  the  main  venous  channel,  the  thyro- 
cervical  artery  and  the  sympathetic  nerve  as  does  the  thoracic 
duct  in  the  later  (16  mm.)  stages. 

In  my  opinion  the  so-called  '  outgrowths'  arising  from  the  main 
venous  trunks  are  the  terminals  of  dorso-medial  tributary  branches 
entering  the  same,  and  have  nothing  to  do  with  the  thoracic 
duct.  They  are  part  of  the  pre vertebral  capillary  plexus  in  rela- 
tion in  this  stage  to  the  dorso-medial  surface  of  the  main  venous 
channels,  as  described  in  detail  in  the  second  part  of  this  paper 
dealing  with  the  development  of  the  preazygos  segment  of  the  thor- 
acic duct  (supra,  p.  84).  This  opinion  is  based  on  the  fact  that  in 
many  14  mm.  embryos  sections  through  this  region  show  the  so- 
called  '  venous  outgrowth'  and  the  thoracic  duct  approach  of  the 
jugular  lymph  sac  coexisting  side  by  side. 

As  previously  described  in  detail  (supra,  pp.  56  to  77)  the  thor- 


160  SYSTEMIC   LYMPHATIC   VESSELS    IN  DOMESTIC   CAT 

acic  duct  approach  of  the  jugular  lymph  sac,  in  certain  typical  14 
mm.  embryos,  extends  as  a  curved  blunt  conical  process  meso- 
caudad  for  some  distance  between  the  main  vein  and  the  thyro- 
cervical  artery,  towards  the  interval  between  the  former  and  the 
sympathetic  nerve,  where  it  ends  blindly.  Mesad  of  the  thoracic 
duct  approach  the  internal  and  common  jugular  veins  receive  a 
number  of  dorso-medial  tributary  radicles  of  the  above  mentioned 
prevertebral  venous  plexus.  Now,  it  will  depend  altogether  upon 
the  degree  of  development  of  any  particular  embryo,  and  the  selec- 
tion of  the  sections,  as  to  whether  both  the  thoracic  duct  approach 
and  the  dorso-medial  tributary  terminal  appear  side  by  side  in  the 
same  field,  or  whether  one  or  the  other,  or  both  are  absent  at  the 
particular  level  examined.  Thus  in  a  14  mm.  embryo  (series  122, 
slide  ix,  section  28,  fig.  58),  the  dorso-medial  tributary  (16)  of  the 
main  vein  (left  internal  jugular,  25)  together  with  the  thoracic 
duct  approach  of  the  jugular  lymph  sac  (12),  are  both  present  in 
the  typical  relation  to  the  thyro-cervical  artery  (24)  and  the  sym- 
pathetic nerve  (1).  Traced  back  in  series  122  to  section  21  of 
slide  ix  (fig.  57)  the  thoracic  duct  approach  (12)  is  seen  to  arise 
from  the  dorso-mesal  aspect  of  the  caudal  end  of  that  portion  of 
the  jugular  lymph  sac,  which,  as  the  terminal  of  the  ventral  division 
of  the  entire  structure,  forms  the  jugular  approach  (13). 

But  since  in  section  28  of  slide  ix  of  series  122,  this  portion  of  the 
future  thoracic  duct  (lymph  sac  segment)  is  present  in  the  classical 
position  between  thyro-cervical  artery  and  sympathetic  nerve, 
dorsal  to  the  common  jugular  vein,  together  with  the  well  developed 
dorso-medial  venous  tributary  (16),  it  must  become  evident  that 
the  latter  cannot  be  regarded  as  a  'venous  outgrowth'  represent- 
ing the  anlage  of  the  thoracic  duct,  since  it  is  manifestly  impossible 
to  include  the  'anlage'  of  a  structure  and  the  actual  structure  it- 
self side  by  side  in  a  single  section. 

As  a  matter  of  fact,  a  selection  of  sections  in  this  neighborhood 
in  series  122  (14  mm.)  will  furnish  all  possible  combinations  of  the 
venous  dorso-medial  tributary  of  the  internal  and  common  jugular 
vein  and  of  the  thoracic  duct  approach  of  the  jugular  sac. 

The  two  structures,  as  can  be  clearly  seen,  both  occupy  in  sec- 
tions at  the  proper  level  the  topographical  position  along  the  dor- 


SUMMARY  AND   CONCLUSIONS 


161 


sal  aspect  of  the  main  vein  and  between  the  thyro-cervical  artery 
and  sympathetic  nerve,  which  has  been  alone  employed  as  the 
basis  of  the  conclusion  that,  in  comparing  the  14  mm.  and  16  mm. 
embryo,  the  thoracic  duct  develops  from  a  portion  of  the  dorso- 
medial  plexus,  secondarily  split  off  from  the  main  vein. 

Thus,  for  example,  the  series  122  under  discussion,  if  employed 
for  purposes  of  topographical  comparison  with  a  16  mm.  embryo, 
should  be  represented  by  the  following  sections: 


SERIES 

SLIDE 

SECTION 

FIGURE 

1  

122 

ix 

21 

57 

2  

122 

ix 

28 

58 

3  

122 

x 

7 

59 

4                           

122 

x 

9 

60 

5  

122 

x 

12 

61 

6  

122 

x 

13 

62 

1.  It  will  be  seen  that  in  section  21  of  slide  ix  (fig.  57),  the  inter- 
val between  thyro-cervical  artery  (24}  and  sympathetic  nerve  (1) 
is  occupied  by  the  thoracic  duct  approach  (12)  directed  meso-cau- 
dad  from  the  jugular  lymph  sac. 

2.  In  section  28  of  the  same  slide  (fig.  58),  the  thoracic  duct 
approach  (12)  has  separated  from  the  sac,  and  appears,  as  the  free 
terminal  of  the  future  adult  duct,  mesad  to  the  thyro-cervical 
artery    (24)-     Further   dorso-mesad  is  a  venous  tributary    (16) 
approaching  the  main  vein .     Elements  of  the  mesal  peri-  and  inter- 
neural  venous  plexus  are  also  seen. 

3.  Section  7  of  slide  x  (fig.  59)  shows,  in  the  interval  between  the 
thyro-cervical  artery  (24)  and  the  sympathetic  nerve  (1)  the  sec- 
tion of  the  thoracic  duct  approach  (12)  close  to  the  dorsal  circum- 
ference of  the  common  jugular  vein  (26). 

4.  In  section  9  of  the  same  slide  (x)  (fig.  60),  the  blind  end  of 
the  thoracic  duct  approach  (12)  is  still  seen  on  the  mesal  side  of 
the  thyro-cervical  artery  (24),  while  further  mesad  the  common 
jugular  vein  (26)  receives  the  terminals  of  the  dorso-medial  venous 
plexus.     Here,  in  other  words,  the  Venous  outgrowths'  or  'an- 
lages  of  the  thoracic  duct,'  and  the  thoracic  duct  approach  of  the 


162  SYSTEMIC  LYMPHATIC  VESSELS  IN  DOMESTIC  CAT 

jugular  lymph  sac  appear  side  by  side,  dorsal  to  the  left  common 
jugular  vein,  between  the  thyro-cervical  artery  and  the  sympa- 
thetic nerve. 

5.  Section  12  of  the  same  slide  (fig.  61)  is  caudal  to  the  blind  ter- 
minal of  the  thoracic  duct  approach.     A  radicle  of  the  dorso-med- 
ial  venous  plexus  (16)  lies  close  to  the  dorsal  circumference  of  the 
common  jugular  vein  (26}  between  the  thyro-cervical  artery  (24) 
and  the  sympathetic  nerve  (1),  approximately  in  the  situation 
occupied  in  the  sections  further  cephalad  by  the  terminal  of  the 
thoracic  duct  approach. 

6.  In  the  following  section  (fig.  62)  this  venous  tributary  opens 
into  the  main  vein. 

A  comparison  of  the  structures  labelled  respectively  16  and  12 
in  figs.  61  and  59  will  show  their  close  topographical  correspondence 
and  will  suffice  to  indicate  how  easily  the  latter,  a  valid  portion  of 
the  future  thoracic  duct,  might  be  confused  with  the  former,  a 
dorso-medial  venous  terminal.  Hence,  in  comparing  successive 
stages,  the  greatest  care  is  necessary  in  order  to  avoid  the  mistake 
of  considering  a  lymphatic  channel  of  the  later  period  to  be  the 
direct  derivative  of  a  'venous  outgrowth'  as  seen  in' an  earlier  em- 
bryo. Other  embryos  of  this  stage  will  give  equally  conclusive 
pictures  of  the  juxtaposition  of  thoracic  duct  approach  (12}  and 
dorso-medial  venous  tributary  (16)  in  their  various  mutual  rela- 
tions (figs.  41,  42,  49,  50,  55). 

Of  course,  caudal  to  the  level  at  which  in  this  stage  the  thoracic 
duct  approach  ends  blindly,  and  before  the  independent  lymphatic 
channels,  which  are  subsequently  (15  mm.  and  15.5  mm.)  to  join 
it,  are  developed,  the  sections  will  only  show  the  dorso-medial 
venous  branches  entering  the  main  channel 

But  these  venous  terminals  of  a  well  defined  plexus  are  in  no 
sense  '  outgrowths'  from  the  veins,  nor  should  they  be  considered 
as  anlages  of  a  lymphatic  structure  which  does  not  appear  in  the 
particular  section  figured,  because  it  has  not  as  yet  developed  at 
that  particular  level,  although,  as  in  the  case  in  point,  it  may  be 
perfectly  evident  and  coexisting  with  the  'venous  outgrowths' 
few  sections  further  cephalad  in  the  same  embryo. 

The  venous  plexuses,  both  in  the  prevertebral  and  in  the  ventral 


SUMMARY  AND   CONCLUSIONS  163 

mediastinal  region,  which  form  the  basis  for  the  extraintimal  lym- 
phatic channel  development  in  the  correlated  segments  of  the 
thoracic  ducts,  are  sufficiently  described  above  (p.  85). 

There  is  no  question  that  the  internal  and  common  jugular  veins 
and  the  innominate  vein  receive,  along  their  mesal  and  dorso- 
mesal  aspects  during  the  13  and  14  mm.  stage,  numerous  tributaries 
of  these  two  plexuses,  as  indicated  above  schematically  in  fig.  101. 
These  terminals  cannot,  however,  be  interpreted  as  '  outgrowths' 
of  the  main  venous  line,  constituting  the  venous  anlages  of  the 
thoracic  duct  in  this  region  and  subsequently  uniting  to  form  the 
continuous  channel  of  this  duct  in  its  preaortic  segment.  They 
are  a  direct  caudal  continuation  of  the  extensive  inter-  and  peri- 
neural  venous  plexus  connected,  cephalad  of  the  thoracic  duct 
level,  with  the  mesal  aspect  of  the  internal  jugular  vein  through- 
out nearly  its  entire  extent. 

The  elements  of  these  early  venous  plexuses  serve  as  lines  of 
extraintimal  perivenous  lymphatic  development. 

Both  in  the  prevertebral  region  cephalad  of  the  aortic  arch  and 
in  the  ventral  mediastinal  area,  as  above  described  (pp.  84  to  110) 
the  extraintimal  anlages  of  both  channels,  the  preazygos  segment 
of  the  thoracic  duct  dor  sally,  and  the  mediastinal  trunk  ventrally, 
can  be  followed  in  the  proper  stages  from  their  earliest  inception 
to  their  full  completion  and  union  with  each  other. 

The  lymphatic  channel  system  in  both  areas,  as  in  all  other 
regions  of  the  body,  is  at  first  very  extensive  and  plexiform,  com- 
posed of  a  larger  number  of  intercommunicating  spaces.  Later 
the  definite  channel,  smaller  in  cross-cut  area  and  more  direct 
in  course,  crystallizes  along  definite  static  lines  out  of  the  pre- 
existing lymphatic  network,  just  as  we  now  know  that  haemal 
channels  do.  In  other  words,  the  systemic  lymphatic  channels, 
as  would  be  expected,  repeat  in  their  development  the  ontogenetic 
stages  of  the  ha3mal  channels.  Both  sets  of  vessels,  lymphatic 
as  well  as  haemal,  result  from  the  condensation  of  an  antecedent 
plexus  along  definite  and  determined  lines  and  thus  give  rise  to 
the  characteristic  vessels  of  the  adult. 

In  this  entire  process  there  is  never  a  question  of  the  direct 
implication  of  a  vein  in  the  formation  of  a  'ymphatic  space.  The 


164  SYSTEMIC  LYMPHATIC  VESSELS  IN  DOMESTIC   CAT 

majority  of  the  spaces  develop,  as  above  described,  extraintimally 
along  or  around  avenule,but  at  the  same  time  a  considerable  num- 
ber of  these  spaces  develop  as  independent  mesenchymal  clefts 
not  directly  related  to  a  degenerating  embryonic  vein.  The  em- 
bryonic history  of  this  portion  of  the  mammalian  lymphatic  sys- 
tem, up  to  the  junction  of  the  completed  preazygos  segments  of 
the  thoracic  ducts,  including  their  ventral  mediastinal  tributary, 
with  the  thoracic  duct  approaches  of  the  left  and  right  jugular 
lymph  sacs,  is,  as  above  stated,  clearly  shown  in  cat  embryos  of 
between  13  and  15.5  mm.  and  need  not  be  repeated  he^e. 

Comparison  of  the  13  and  14  mm.  stages  with  slightly  older 
embryos  (15  mm.)  definitely  proves  the  correctness  of  the  view 
just  expressed.  In  the  course  of  further  development  the  thoracic 
duct  approach,  turning  ventro-mesad  into  the  neuro-venous  inter- 
val between  sympathetic  nerve  and  common  jugular  vein  in 
proceeding  latero-mesad  across  the  dorsal  aspect  of  the  latter 
vessel,  necessarily  intersects  the  line  of  the  dorso-medial  venous 
tributaries.  Its  blind  terminal  must  exchange  the  position  which 
it  occupies  in  the  earlier  (13-14  mm.)  stages,  lateral  to  the  dorsal 
somatic  venous  branch,  for  one  situated  on  its  mesal  aspect,  if 
the  vessels  are  functional  venous  tributaries  and  not,  as  has  been 
held,  venous  anlages  of  the  future  thoracic  duct  in  this  region.  In 
other  words,  they  should  continue  in  the  later  stages  side  by  side 
with  the  thoracic  duct  more  fully  developed,  if  they  have  not  be- 
come detached  from  the  main  vein  to  form  by  fusion  the  lymphatic 
channel.  This  is  seen  to  be  the  case,  for  example,  in  the  sections 
of  the  15  mm.  cat  embryo  (series  245)  shown  in  figs.  79,  80,  81  and 
82.  The  thoracic  duct  approach  (12)  here  has  extended  further 
meso-ventrad  into  the  recess  between  sympathetic  nerve  (1)  and 
common  jugular  vein  (26)  and  now  lies  on  the  mesal  aspect  of  the 
ventro-medial  venous  tributary  (16)  which  opens  into  the  main 
vein  in  fig.  82.  Fig.  90  shows  clearly  in  the  dorsal  view  of  the 
reconstruction  of  this  embryo  the  lymphatic  channel  (12-85) 
intersecting  at  an  acute  angle  the  coexisting  dorsomedial  tributary 
(16-46). 


SUMMARY   AND   CONCLUSIONS  165 

II.     AZYGOS  SEGMENT  OF  THORACIC  DUCT 

The  genesis  of  the  azygos  segment  of  the  thoracic  ducts  is  in 
my  estimation  the  region  in  which  the  validity  of  divergent  views 
as  to  systemic  lymphatic  development  can  best  be  tested. 

Certain  mechanical  and  genetic  conditions  combine  to  make 
the  investigation  of  the  development  of  the  thoracic  ducts  in  this 
region  perhaps  difficult  in  one  sense,  while  in  another  the  results 
of  thorough  investigation  are  most  conclusive  and  convincing. 

Part  of  the  difficulty  referred  to  lies  in  the  relatively  small 
amount  of  the  retro-  and  peri-aortic  space  available  for  the  develop- 
ment both  of  the  azygos  veins  and  of  the  subsequent  lymphatic 
ducts  replacing  the  same  to  a  large  extent.  Again,  the  process 
of  systemic  lymphatic  development  in  this  region  appears  to  pro- 
ceed with  great  rapidity.  The  first  anlages  of  the  thoracic  ducts 
in  a  given  stage  are  succeeded  in  stages  only  slightly  older  by  well 
marked  longer  segments  of  the  future  lymphatic  channel.  On  the 
other  hand,  the  observer  has  the  advantage  of  dealing  with  a  cir- 
cumscribed region  and  with  axial  venous  trunks,  which,  both  in 
their  main  line  and  in  their  tributaries,  are  remarkably  constant, 
regular  and  easily  distinguished. 

As  above  stated,  in  the  earlier  stages  a  ventral  tributary  plexus 
of  the  azygos  veins  drains  the  periaortic  region.  In  later  stages 
this  ventral  venous  plexus  in  large  part  disappears,  a  bilateral 
lymphatic  duct  occupying  its  former  place.  The  two  conditions 
cover  each  other  absolutely. 

No  one,  possessing  a  knowledge  of  the  embryonic  venous  devel- 
opment of  the  cat,  can  examine  a  number  of  injections  of  the  thor- 
acic ducts  and  azygos  veins  of  the  adult  animal  without  becoming 
convinced  that  in  course  of  development  the  thoracic  duct  complex, 
caudal  to  the  aortic  arch-level,  replaces  a  large  part  of  the  embry- 
onic azygos  venous  system,  and  comes  to  occupy  absolutely  its  topo- 
graphical position  and  relation  to  surrounding  structures.  The 
relation  of  the  dorsal  intersegmental  aortic  branches  to  the  inter- 
azygos  venous  anastomosis  of  the  embryo,  compared  with  the 
intercostal  arteries  of  the  adult  perforating  through  the  meshes 
of  the  plexiform  lymphatic  channel  of  the  thoracic  ducts,  will  alone 
absolutely  demonstrate  this  mutual  topographical  correspondence. 


166  SYSTEMIC  LYMPHATIC  VESSELS  IN  DOMESTIC  CAT 

The  only  question  at  issue  is  the  determination  of  the  genetic 
processes  through  which  the  embryonic  azygos  venous  plexus  is 
replaced  by  the  lymphatic  network  of  the  thoracic  ducts  in  the 
adult. 

Some  observers  have  derived  this  portion  of  both  ducts  directly 
from  the  ventral  aspect  of  the  azygos  veins  by  comparing  tran- 
sections  of  14  mm.  and  16  mm.  embryos,  and  finding  in  the  former 
ventral  tributaries  of  the  main  channels,  whose  place  in  the  latter 
is  occupied  by  the  thoracic  ducts.  They  hence  conclude  that 
the  ventral  azygos  plexus,  forming  'the  veno-lymphatic  anlages' 
of  the  thoracic  ducts,  separates  at  numerous  points  from  the  parent 
vein,  and  that  the  resulting  detached  portions  of  the  originally 
continuous  venous  plexus,  secondarily  unite  to  form  the  channel 
of  the  thoracic  ducts.  The  latter  structures  are  therefore,  in  their 
estimation,  direct  derivatives  of  the  azygos  veins  and  their  tribu- 
taries. 

The  preceding  pages  give  my  reasons  for  regarding  this  replace- 
ment as  having  occurred  in  course  of  the  development  of  the  thor- 
acic ducts  by  confluence  of  numerous  isolated  mesenchymal  spaces, 
formed  along  and  around  the  azygos  veins  and  their  ventral  trib- 
utaries, but  genetically  independent  of  the  latter  and  lined  by  an 
endothelium  not  derived  from  the  pre-existing  haemal  endothe- 
lium. 

In  the  region  under  discussion  these  mesenchymal  clefts  develop, 
owing  to  local  conditions,  very  largely  as  extraintimal  or  peri- 
venous  spaces  accompanying  and  surrounding  the  branches  of  the 
retrograding  ventromedial  azygos  plexus.  The  resulting  thoracic 
ducts  thus  come  to  occupy  the  place  formerly  filled  by  the  ventral 
azygos  venous  network,  and  later  are  led  into  direct  ventral 
contact  with  the  main  azygos  veins,  which  they  in  their  further 
growth  to  a  large  extent  secondarily  replace. 

In  the  early  (11-12  mm.  stage)  the  azygos  veins  receive  on  their 
ventral  and  ventro-medial  aspect  the  terminals  of  a  venous  plexus 
originating  in  the  retro-  and  peri-aortic  mesenchyme.  While  the 
individual  embryos  offer  many  striking  pictures  at  various  levels, 
I  believe  that  my  purpose  of  demonstrating  the  genesis  of  the 
thoracic  ducts  in  this  area  will  best  be  accomplished  by  taking 


SUMMARY  AND   CONCLUSIONS  167 

section's  in  successive  stages  which  will  present  approximately  the 
same  topographical  picture,  allowing  for  the  necessary  changes 
consequent  on  increasing  development.  The  area  to  which  I  thus 
desire  to  call  detailed  attention  is  the  mesenchymal  tissue,  situated 
on  the  right  side  of  the  thoracic  aorta,  between  this  vessel  and  the 
mesal  aspect  of  the  right  azygos  vein,  ventral  to  one  of  the  right 
dorsal  somatic  (intercostal)  branches  of  the  aorta,  and  under  cover 
of  the  dorsal  surface  of  the  oesophagus. 

These  limitations,  as  is  well  known,  define  the  position  of  this 
portion  of  the  main  thoracic  duct  of  the  adult,  and  consequently 
the  development  of  this  structure,  however  produced,  must  run 
its  course  in  this  situation.  The  successive  stages,  which  in  my 
opinion  definitely  and  conclusively  prove  the  independent  extra- 
intimal  anlage  of  this  portion  of  the  right  thoracic  duct,  may  be 
grouped  as  follows,  and  referred  to  selected  illustrations  above  de- 
scribed in  the  body  of  the  text  in  detail : 

A.  Venous  stage.  (Embryos  from  10  mm.  to  13  mm.).  Illus- 
trations in  body  of  text:  figs.  194  to  203. 

The  sections  show  an  extensive  ventral  and  ventromedial  azy- 
gos tributary  plexus. 

B  Stage  of  replacement  of  ventral  azygos  venous  plexus  by  inde- 
pendently developed  perivenous  or  extraintimal  lymphatic  anlages 
which  accompany  and  surround  the  branches  of  the  antecedent 
venous  network,  and  form  the  first  anlages  of  the  azygos  segment  of 
the  thoracic  ducts.  (Embryos  from  13  to  14  mm.)  Illustrations 
in  body  of  text:  figs.  204  to  213;  247  to  251. 

1.  The  earliest  anlages  of  the  future  thoracic  ducts  are  seen  in 
certain  sections  of  the  thoracic  region  in  embryos  between  12  and 
13  mm.  crown-rump  measure.  I  have  found  these  early  traces 
almost  exclusively  on  the  right  side,  the  sinistral  position  of  the 
aorta  appearing  to  delay  their  development  on  the  left  side.  They 
make  their  first  appearance  as  delicate  endothelial-lined  extremely 
sparse  and  widely  separated  independent  mesenchymal  clefts, 
at  some  distance  ventral  to  the  main  right  azygos  trunk  and  near 
the  right  lateral  wall  of  the  aorta. 

At  first  they  are  not  clearly  related  to  the  co-existing  ventro- 
medial tributaries  of  the  azygos.  But  they  soon  extend  to  involve 


168  SYSTEMIC  LYMPHATIC  VESSELS  IN  DOMESTIC  CAT 

these  in  the  characteristic  manner  above  detailed,  and  continue 
to  develop  as  extraintimal  or  perivenous  lymphatic  spaces  grad- 
ually replacing  the  shrinking  ventral  azygos  plexus. 

2.  In  the  succeeding  stage  (13+  mm.)  the  aorta  sinks  more 
deeply  into  the  interazygos  interval  and  is  spanned  on  its  dorsal 
aspect  by  the  horse  shoe  of  the  abundant  supra-aortic  cross  anas- 
tomosis between  the  azygos  trunks  of  the  two  sides.     The  periven- 
ous extraintimal  lymphatic  spaces  surrounding  and  accompany- 
ing the  ventral  azygos  tributaries  have  increased  in  size,  and  a  few 
spaces  of  the  same  character  begin  to  make  their  appearance  along 
the  ventro-lateral  aspect  of  the  main  azygos  veins. 

3.  In  the  13.5  mm.  embryo  the  extraintimal  anlages  replacing 
the  ventro-medial  azygos  tributaries  have  increased  in  number, 
united  with  each  other  to  form  a  series  of  longer  continuous  seg- 
ments, and  have,  following  the  lead  of  the  venules  which  they  are 
replacing,  approached  nearer  to  the  ventral  aspect  of  the  main 
azygos  veins,  and  appear  more  closely  interlocked  with  the  ventro- 
medial  tributaries  of  the  latter. 

C.  14  mm-  stage.     Illustrations  in  body  of  text :  figs.  214  to  240. 

The  most  instructive  and  conclusive  pictures  are  obtained  in 
embryos  of  approximately  this  crown-rump  measure. 

The  sections  are  clearer  and  most  unmistakable  in  their  meaning 
and  the  individual  spaces  have  become  confluent  for  longer 
stretches,  representing  longer  segments  of  the  thoracic  duct  chan- 
nel which  is  subsequently  to  be  formed  by  their  continued  elon- 
gation and  fusion  with  each  other.  This  becomes  clearly  apparent 
in  contrasting  the  ventral  view  of  the  reconstruction  of  series  76 
(13.5  mm.)  with  that  of  series  214  (14  mm.)  shown  in  figs.  188  and 
190. 

The  diffuse  and  scattered  elements  of  the  parazygos  lymphatic 
plexus  anlages  in  the  13.5  mm.  stage  have,  in  the  14  mm.  embryo, 
become  condensed  and  united  into  longer  segments  representing 
the  future  line  of  right  axial  prevertebral  lymphatic  drainage.  It 
is  noteworthy,  as  an  important  fact,  that  notwithstanding  the 
clear  development  of  unmistakable  longer  segments  of  the  future 
right  thoracic  duct,  these  anlages  are  still  placed  at  some  distance 
ventro-mesal  to  the  right  azygos  vein  and  ventral  to  the  inter- 
segmental  arteries. 


SUMMARY  AND   CONCLUSIONS  169 

The  14  mm.  embryo  represents  thus  in  general  the  full  develop- 
ment of  the  histological  picture  of  secondary  replacement  of  a 
decadent  embryonic  venous  plexus  by  the  secondarily  developed 
extraintimal  perivenous  lymphatic  spaces  and  channels. 

The  following  conditions  have  been  noted  in  individual  sec- 
tions : 

a.  Ventro-medial  tributary  of  right  azygos  connected  with  main 
vein,  detached  on  left  side. 

Anlage  of  right  thoracic  duct  lateral  to  right  ventral  azygos 
tributary . 

b.  Ventro-medial  tributaries  of  both  azygos  veins  surrounded  by 
extraintimal  anlages  of  both  ducts. 

c.  Ventro-medial  tributaries  detached  and  surrounded  by  ex- 
traintimal anlages  of  thoracic  ducts  on  both  sides. 

d.  Ventro-medial  tributaries  in  connection  with  both  azygos 
veins  and  accompanied  by  ventro-lateral  lymphatic  anlages  on 
both  sides. 

e.  Azygos  veins  without  ventro-medial  branches  or  their  rem- 
nants and  accompanied  on  both  sides  by  the  thoracic  duct  anlages 

/.  Azygos  veins  with  ventro-medial  tributaries  without  duct 
anlages. 

g.  Azygos  veins  without  either  ventro-medial  tributaries  or 
thoracic  duct  anlages. 

D.  Later  transitional  lymphatic  stages.  Illustrations  in  body  of 
text:  figs.  252  to  258. 

In  the  15  and  15.5  mm.  embryo  three  further  developmental 
characters  appear: 

a.  The  earlier  more  redundant  and  plexiform  lymphatic  anlages 
condense  into  a  definite  channel  of  relatively  smaller  caliber. 

b.  The  central  remnants  of  the  atrophied  embryonic   vein, 
around  which  the  lymphatic  anlages  developed,  have  to  a  large 
extent  disappeared,  leaving  the  lymphatic  lumen  clear. 

c.  The  individual  and  originally  separate  segments  of  the  lym- 
phatic channels  have  united  into  segments  of  greater  length,  and 
have  approached  more  closely  to  the  ventral  surface  of  the  main 
azygos  trunks.     The  definition  of  a  right  and  left  lymphatic  trunk 
with  supra-aortic  cross  anastomoses  is  beginning  to  appear,  al- 


170  SYSTEMIC  LYMPHATIC  VESSELS  IN  DOMESTIC  CAT 

though  the  former  is  still  the  larger  and  better  defined.  It  occu- 
pies the  original  position  between  aorta  and  ventromesal  surface 
of  the  right  azygos  vein,  ventral  to  the  intercostal  artery,  dorsal 
to  the  oesophagus. 

E.  Definite  lymphatic  stage.  From  the  16  mm.  embryo  on. 
Illustrations  in  body  of  text :  figs.  259  to  262 ;  figs.  265  to  270. 

Here  all  the  thoracic  duct  anlages  have  united  into  the  contin- 
uous and  connected  plexiform  channel  of  the  thoracic  ducts, 
ventral  to  the  azygos  trunks,  dorsal  to  the  aorta. 

The  early  independent  genetic  history  of  the  spaces,,  which  I 
have  above  described  as  the  first  anlages  of  the  thoracic  duct 
channels  in  the  embryos  of  the  cat,  and  the  fact  that  in  subsequent 
stages  they  appear  consistently  and  in  every  possible  combination 
as  extraintimal  or  perivenous  mesenchymal  spaces,  following  and 
surrounding  the  branches  of  the  ventral  azygos  plexus,  exclude  to 
my  mind  the  possibility  of  regarding  them  as  derived  directly  from 
ventral  azygos  venous  plexus,  or  from  socalled  'venous  outgrowths' 
of  the  main  azygos  trunks,  subsequently  detached  from  the  parent 
trunks. 

In  the  foregoing  genetic  history  of  part  of  the  thoracic  duct 
lymphatic  plexus,  by  fusion  of  extraintimal  and  perivenous  mesen- 
chymal spaces,  accompanying  and  surrounding  certain  of  the  ven- 
tral venous  tributaries  of  the  right  azygos  trunk,  the  following 
points  should  be  noted: 

1.  The  portion  of  the  entire  adult  thoracic  duct  complex  here 
considered  develops  in  its  earliest  stages  at  some  distance  ventro- 
mesad  to  the  right  azygos  vein.     It  only  subsequently,  by  extend- 
ing proximad  along  the  venule  which  it  replaces,  reaches  the  posi- 
tion in  close  relation  to  the  ventral  surface  of  the  azygos  which  it 
occupies  in  the  16  mm.  stage. 

2.  In  the  13.5  and  14  mm.  embryos  the  radicles  of  the  ventro- 
medial  tributary  plexus  are  in  the  process  of  being  surrounded  by 
the  growing  perivenous  extraintimal  lymphatic  spaces  which  are 
approaching  along  this  line  the  ventral  surface  of  the  azygos,  but 
in  the  14  mm.  stage  have  not  yet  acquired  this  position.     The  16 
mm.  embryo  shows  the  lymphatic  anlages  in  their  definite  relation 
to  the  azygos  trunk,  and  the  primitive  ventral  venous  tributary 


SUMMARY   AND   CONCLUSIONS  171 

along  which  the  lymphatic  spaces  expanded  to  reach  this  position, 
has  disappeared.  The  successive  stages  of  this  process  can  be 
followed  in  such  detail  and  in  such  conclusive  preparations  that  all 
doubt  as  to  the  accuracy  of  the  statements  here  made  seems  to  me 
to  disappear.  It  is  merely  a  question  of  suitable  material,  accur- 
ately fixed,  sectioned  and  stained,  and  sufficiently  abundant  to 
pffer  complete  corroboration  in  a  number  of  series  of  the  same  age. 
There  can  then  be  no  question  as  to  the  genetic  principles  involved. 

3.  The  portion  of  the  thoracic  duct,  whose  genetic  history  has 
just  been  outlined,  forms  only  a  component  of  the  entire  lym- 
phatic complex  entering  into  the  formation  of  the  adult  duct.  Two 
other  equivalent  components  combine  with  it  to  produce  the  adult 
conditions,  viz.,  a  corresponding  segment  on  the  left  side,  devel- 
oped in  the  same  way  in  association  with  the  ventral  tributary 
plexus  of  the  left  azygos  vein,  and  an  intermediate  plexiform  lym- 
phatic reticulum  which  arises  as  the  result  of  fusion  of  extraintimal 
lymphatic  spaces  formed  along  the  ventral  aspect  of  the  supra- 
aortic  interazygos  venous  plexus. 

In  addition  to  these  three  cardinal  elements  entering  into  the 
organization  of  the  adult  thoracic  ducts,  these  channels,  when  once 
they  have  gained  their  position  ventro-mesad  to  the  azygos  trunks, 
grow  partly  by  their  own  expansion,  partly  by  addition  of  num- 
erous new  extraintimal  lymphatic  spaces  which  form  along  the 
azygos  veins,  expecially  on  the  left  side. 

The  eventual  reduction  of  the  left  azygos  vein,  and  of  the  cau- 
dal part  of  the  right  trunk,  by  transferance  of  the  blood  current 
to  the  vertebral  chain,  accounts  for  the  topographical  relations 
of  the  replacing  thoracic  duct  complex  of  the  adult. 


172  SYSTEMIC  LYMPHATIC  VESSELS  IN  DOMESTIC  CAT 

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Am.  Jour.  Anat.,  vol.  1,  1902,  pp.  367-389. 

1904  On  the  development  of  the  superficial  lymphatics  in  the  skin  of 
the  pig.  Am.  Jour.  Anat.  vol.  3,  pp.  183-195. 

1905  The  development  of  the  lymphatic  nodes  in  the  pig,  and  the 
relation  to  the  lymph  hearts.  Am.  Jour.  Anat.,  vol.  4,  pp.  355-389. 

1908  Further  evidence  on  the  origin  of  the  lymphatic  endothelium  from 
the  endothelium  of  the  blood  vascular  system.  Anat.  Rec.,  vol.  2,  pp. 
46-54.        » 

1909  The  lymphatic  system  in  human  embryos,  with  a  consideration 
of  the  morphology  of  the  system.  Am.  Jour.  Anat.,  vol.  9,  pp.  43-90. 

SALA,  LUIGI,  1900  Sullo  sviluppo  dei  cuori  linfatici  e  dei  dotti  toracici  nell 
embrione  di  polio,  Ricerche  fatta  nel  Laborat.  di  Anat.  norm,  della  R. 
Univ.  di  Roma,  vol.  7. 

SCHULTE,  H.  v.  W.,  1907    The  range  of  variations  in  monotremes  and  Australian 
Marsupials.  Am.  Jour.  Anat.,  vol.  6,  Anat.  Rec.,  vol.  1,  pp.  243-36. 
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SCHULTE,  H.  v.  W.,  AND  TILNEY,  FRED.  1909  Note  on  the  organization  of  the 
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SILVESTER,  C.  F.  1910  On  the  presence  of  permanent  lymphatico-venous  com- 
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BIBLIOGRAPHY  175 

STROMSTEN,  FRANK  A.  1910  A  contribution  to  the  anatomy  and  development  of 
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1911  On  the  relations  between  the  mesenchymal  spaces  and  the  devel- 
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SWAEN,  A.,  ET  BRACHET,  A.  1899-1900  fitude  sur  les  premiers  phases  du  de"vel- 
oppement  des  organs  derives  du  mesoblast  chez  lespoissons  te'leostiens. 
Arch,  de  Biologic,  16. 

THOMA,  R.  1893  Untersuchungen  liber  die  Histogenese  und  Histomechanik  des 
Blutegefasssystems,  Stuttgart. 


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